Schizosaccharomyces pombe , a member of the Taphrinomycotina subphylum, is evolutionarily much too far apart from the eight other yeasts—all Saccharomycotina —to expect common traces in its genome. Indeed, the evolution of the Schizosaccharomyces genomes, with their near extinction of transposons, has only been recently addressed Rhind et al. Nevertheless, the original S. The origin of the massive intron loss in the latter group needs to be further elucidated, but it was derermined that, solely within the Saccharomycetaceae family where this has been studied, the rate of intron loss exceeds that of intron gain by two orders of magnitude Hooks, Deleneri and Griffiths-Jones Initially, L.
Multidimensional comparisons only became possible when the sequences of C. This work revealed interesting aspects in terms of sequence divergence. Pairwise comparisons of predicted products from all orthologs between any two yeast species generated mono-modal distributions, typical of homogenous populations. Variances were large, as expected from the different selective pressures acting on the different proteins, but means or medians could be used to estimate gross evolutionary distances between any two yeast genomes whose nucleotide sequences were not usable because of saturated mutational changes.
In comparison, the pairwise comparisons between predicted products from paralogous genes within a given genome generated bi-modal distributions, typical of heterogeneous populations see below. The high sequence divergence between yeasts illustrates their long evolutionary separations, even between members of the same genus. Similarly, the Saccharomycetaceae family alone exceeds, in terms of amino acid sequence divergence, that covering all vertebrates Dujon Also, budding yeasts the Saccharomycotina subphylum of Ascomycota contain many other families.
Furthermore, yeast species also exist in other fungal subdivisions. When discussing genome evolution in yeasts, we must, therefore, take this dimension into consideration. Except for very specific cases, yeast species are not closely related to one another, as is often erroneously stated in the literature. Beside sequence divergence and loss of synteny, yeast genomes also differ from one another by the presence or absence of some protein-coding gene families.
This is obviously not unique to them; all living lineages share the same phenomenon. However, the broad evolutionary spectrum of yeasts offers interesting cases to examine the mechanisms acting at various time scales.
Within the Saccharomycetacea family Souciet et al. They generally represent about two-thirds or even less of the total number of protein families present in each species. The rest are composed of protein families only present in subsets of species, in various combinations, and sometimes in only one species, forming what is called species-specific genes or, if without a homolog in any organism, orphan genes.
Defining their origin and function is a very challenging task. On a shorter evolutionary scale, the same phenomenon exists, only quantitatively reduced. Similar figures apply for the Saccharomyces sensu stricto species Libkind et al. The frequent loss of genes from yeast genomes is consistent with the low frequency of essential genes in S.
However it must also be related to the preponderance of clonal propagation versus sexual reproduction in most lineages. The losses may result from sequence alteration leading to pseudogenes Lafontaine and Dujon or, more frequently, from the entire deletion of the corresponding DNA segment.
Comparisons between genomes of conserved synteny indicate the quantitative importance of the phenomenon, and show that genes are mostly lost individually. Interestingly, functionally co-ordinated genes tend to be lost in parallel, although dispersed in a genome Hittinger et al.
Remarkably, gene loss may confer novel adaptive functions by alteration of regulatory networks, as observed in some pathogens Gabaldon et al. It is now clear that such gains result from the combination of several mechanisms, the most frequent being the duplications, but horizontal acquisitions see below , capture from non-chromosomal sources and de novo gene creation were also described.
In contrast to these last mechanisms, duplications do not expand protein family repertoires but generate families of paralogous genes.
Next to the whole-genome duplication mentioned above that occurred in distant ancestry within the Saccharomycetaceae family, dispersed gene paralogs and tandem gene arrays have been observed in all yeast genomes sequenced so far, generating a universal redundancy Butler et al. The large segmental duplications, common to genomes of many eukaryotes including man, remain scarce in natural yeast genomes if one ignores subtelomeric regions.
These duplications, however, are easily obtained experimentally, indicating that the mechanisms for their formation are active in yeasts Koszul et al. In specific instances, massive amplifications forming macrotene chromosomes were also obtained Thierry et al.
The bi- or plurimodal distributions of sequence identity between paralogous gene products Dujon et al. Some correspond to very ancestral gene duplications, conserved across enormous numbers of successive generations; others are the result of more recent duplications that may or may not be conserved in subsequent generations.
On an intermediate evolutionary range like the one exemplified by the first five protoploid species of the Saccharomycetaceae family studied a few years ago Souciet et al. The remaining genes families were not or were only partially conserved between species, and some showed significant expansions or contractions of gene number.
These figures give us an estimate of the kinetics of evolution of paralogous gene families, within a homogeneous group of yeast genomes with conserved architecture, that can usefully be related to other parameters such as sequence divergence and loss of synteny to better define evolutionary clocks Rolland and Dujon The overall dynamic equilibrium that appears to emerge over evolutionary times from the interplay between gene loss and duplications explains the fourth important surprise of the original S.
Tandem gene arrays showed even faster kinetics of change. In the same five protoploid Saccharomycetaceae species, only eight arrays were entirely conserved compared with an average of 13 9—16 arrays specific to each species total 63 , and 32 others showing partial conservation. Beside duplications, novel genes in yeast chromosomes can also originate from the capture of non-chromosomal elements of the same cell. However, it is the de novo creation of genes that probably represents the most important source of innovation, explaining in part the origin of orphan genes Tautz and Domazet-Loso This mechanism has long been regarded as extremely unlikely if not totally impossible because the mutational transformation of a random sequence into a meaningful sequence has an infinitely low probability Tautz However, random nucleotide sequences do not exist.
In every extant genome or RNA molecule, sequences are copies of pre-existing ones bearing the traces of all historical events, superimposed upon functional constraints. As a result, all nucleotide sequences, coding or not, show significant deviations from randomness, as easily monitored by, for example, dinucleotide frequencies Dujon et al. Genomes, therefore, offer plenty of raw materials out of which novel genes may easily emerge.
A first mechanism is exon-shuffling, i. However, more generally, the widespread translation of non-genic sequences observed by ribosome footprinting is consistent with the idea of a reservoir of protogenes, i.
The S. The reservoir is large. Actual examples supporting this hypothesis remain limited in number so far, but two demonstrable cases of de novo gene creation in S. The latter case is interesting because the new gene extensively studied in S.
Finally, the classical idea of genomes originating from clear, tree-like phylogenies is also being challenged by the most recent data from yeasts.
Horizontal gene transfer has now been recognized as an important source of innovation in many organisms, and yeasts do not escape the phenomenon. Numerous examples of genes from bacterial origin as judged from molecular phylogenies have been found in yeast genomes, most of which correspond to basic metabolic functions. Almost every yeast species sequenced so far has at least one gene of bacterial origin, and very often several. Probably acquired from a Lactococcus- like bacterium in a common ancestor of this family, it encodes a dihydro-orotate dehydrogenase active under anaerobic conditions in contrast to the ancestral mitochondrial enzyme encoded by URA9.
This horizontal transfer is thus one of the evolutionary steps that enabled Saccharomyces species to propagate anaerobically, facilitating alcoholic fermentations. The mechanism of DNA transfer from bacteria to yeasts has not yet been elucidated, but it is probably facilitated by the ecological proximity between the organisms. In addition to single genes, large chromosomal segments of alien origin were also found in yeast genomes for a review, see Morales and Dujon An interesting example is provided by the acquisition of a 17 kb long segment of Zygosaccharomyces baillii inserted in several copies in the genomes of S.
These yeasts assimilate nitrate. Again, the mechanism at the origin of such large introgressions is not yet understood, but it must involve close contact, or perhaps temporary fusion, between cells. Such events are probably rare, but the functional advantages provided by horizontal acquisitions may be so strong that the novel lineages of natural genetically modified organisms rapidly replace the original populations.
Stable cellular fusions, on the other hand, are clearly at the origin of the many hybrid genomes now recognized in yeasts. For a long time regarded as evolutionary dead-ends due to a lack of meiotic fertility, interspecies hybrids are so numerous in yeasts that they must play a significant role for a review, see Morales and Dujon The phenomenon was suspected long ago for the major brewing strain, Saccharomyces pastorianus previously called S.
Beside the natural hybridizations between S. Hybrid genomes were also mentioned in the totally distinct group of Cryptococcus yeasts belonging to the Basidiomycota phylum Boekhout et al. The phenomenon of interspecies hybridization appears so universal that even a type strain such as Saccharomyces bayanus was recently recognized as being a complex interspecies hybrid Libkind et al.
The genetic make-up of hybrid genomes is extremely variable depending on the ploidy of parents and on the post-hybridization events. Cases of hybridizations between two haploid parents, two diploid parents or one of each type have been reported. Triple species hybridization was also encountered. Numerous examples of aneuploidy or partial chromosome loss are observed.
The sequence of the recently isolated osmotolerant yeast Millerozyma sorbitophila was particularly informative because this genome exhibits seven conserved pairs of chromosomes suggesting recent hybridization between two haploid parents , entirely co-linear except for a single reciprocal translocation , but in the process of resolution by a loss-of-heterozygosity mechanism Leh-Louis et al.
One parent is very close but not identical to a known strain of Millerozyma farinose ; the other is unknown. In the hybrid, some pairs of chromosomes have already been entirely or partially converted to homozygous copies of one or the other parent with a bias , forming a chimeric genome of two origins with, interestingly, the ribosomal DNA cluster and the mitochondrial DNA each inherited from a single parent not the same , and a global level of single gene loss reaching 3.
To what extent these processes are driven by functional selection or occur at random remains to be studied. Thus, it is not excluded that, after complete resolution, hybrid genomes of multiple ancestry propagate indefinitely, forming novel species.
Recent results on Lachancea kluyveri , a protoploid species of Saccharomycetaceae carrying a conserved 1 Mb GC-rich introgression from its ancestor, support this idea Friedrich et al. In the absence of such an easily detectable trait, however, it is possible that many more cases of multiple ancestries exist in yeast genomes that have so far escaped our attention. More sequencing will be needed to estimate the actual degree of reticulation in yeast genome evolution. In writing this recollection, I was obviously biased by my own scientific interest.
My colleagues, who also were at the origin of yeast genomics, may emphasize different viewpoints. However, they will certainly reach the same general conclusion: the progress in genomics since the sequencing of S. Obviously, yeasts were not alone in this two-decade long endeavor, but they contributed their share, and perhaps even more. Our understanding about genomes has reached frontiers not even imagined 20 years ago, and the relationship with phenotypes is now based on entirely new concepts in which RNA molecules, metastable equilibria, trans-generational influence and the tuning of biological noise play increasing roles.
It should also not be forgotten that genomes can be edited or even entirely resynthesized at will, only imitating what nature is silently doing. We are probably still at the very beginning of a long journey with outstanding promises.
Technologies and computer science, in their continuing progress, will probably open the gates of as yet unexplored biological dimensions for their own benefit as well. In , following the excitement created by the completion of the S. For the yeasts, we are almost there.
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Jakob Vowinckel, University of Cambridge. Image courtesy of Masur. Wikimedia Commons. Peroxisome red and mitochondrial green fission defects in vps1 fis1 double deletion strain transformed with FIS1. Lefevre, S. Kumar and I. Image courtesy of V. Zayats and J. The distribution of mtDNA green within the mitochondrial network red. Image courtesy of A.
Nakano and K. Cell, actin and nuclear morphology of yeast cells treated with DMSO left and poacic acid right. Localization of active Ras in a wild type strain Image courtesy of S. Colorectal cancer, also known as bowel cancer, is a complex disease that is influenced by multiple genes and environmental factors. Hereditary non-polyposis colorectal cancer is a rare condition, but it is the commonest inherited syndrome that predisposes sufferers to early-onset colorectal cancer.
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