Major Gene Families in Humans and Their Evolutionary History Prof. Yoshihito Niimura Prof. Masatoshi Nei

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1 Major Gene Families in Humans Yoshihito Niimura Tokyo Medical and Dental University and Masatoshi Nei Pennsylvania State University 1 1. Multigene family Contents 2. Olfactory receptors (ORs) 3. OR genes in humans 4. Comparison of OR genes between humans and mice 5. Evolution of OR genes in vertebrates 6. Other chemosensory receptor genes 2 Multigene family 3 The screen versions of these slides have full details of copyright and acknowledgements 1

2 Multigene family Multigene family a group of genes that have descended from a common ancestor and therefor e have similar functions and similar DNA sequences Duplication Pseudogenizati on Divergence X Pseudogene 4 Color vision genes Human color vision is mediated by three light-sensiti ve protein pigments present in the cone cells of the retina; Blue-pigment gene - chromosome 7 Red- and green-pigment genes - chromosome X Red and green pigment genes are 96% identical in amino acid sequence They were generated by recent gene duplication Unequal crossing-over (From Essential Genetics) Color-blindness Normal 5 Color vision genes Gene duplication between red- and green-pigment genes Human Chimpanzee Gorilla Orangutan Gibbon Rhesus Baboon Mangabey Mona Langur Colobus Brown Capucin Squirrel monkey Owl monkey Marmoset Howler monkey Spider monkey Woody monkey Lemur Non-primate eutherian mammals Catarrhine (Old World monkey + apes + human) New world monkey Prosimian Trichromatic? Dichromatic 6 The screen versions of these slides have full details of copyright and acknowledgements 2

3 Most New World monkeys: Color vision genes There is a single pigment gene on X chromosome, but this gene is polymor phic Males Females Major Gene Families in Humans Dichromatic Dichromatic Trichromatic Howler monkey: Full trichromatic 7 Acquisition of full trichromatic vision Color vision genes Human Chimpanzee Gorilla Orangutan Gibbon Rhesus Baboon Mangabey Mona Langur Colobus Brown Capucin Squirrel monkey Owl monkey Marmoset Howler monkey Spider monkey Woody monkey Lemur Catarrhines (Old World monkeys + apes + human) New world monkeys Prosimians Full trichromatic vision arose twice independently in primates 8 Concerted evolution Ribosomal RNA Ancestral species Time Birth-and-death evolution Major histocompatibility complex (MHC) Most gene families Olfactory receptor Species 1Species 2 Species 1Species 2 Concerted evoluti on all member genes of a family evolve as a unit in concert Birth-and-death evolution new genes are created by gene duplication, and some duplicated genes are maintai ned in the genome for a long time, whereas others are deleted or become nonfuncti onal through deleterious mutations 9 The screen versions of these slides have full details of copyright and acknowledgements 3

4 Olfactory receptors 10 Olfaction the sense of smell is essential for the survival of animals The proteins for detecting odor molecules in the environment are olfactory receptors (ORs) OR genes were first identified from rats by Linda Buck and Richard Axel in Nobel Prize in Physiology or Medicine There are ~ 1,000 OR genes in the mammalian genomes (~ 4% of the entire proteomes) The largest multigene family in vertebrates 11 OR genes are mainly expresses in olfactor y epithelia in the nasal cavity Olfactory bulb Cribriform plate Olfactory epithelium Nasal cavity Olfactory bulb Cribriform plate Olfactory nerve Receptor cell axons (to olfactory bulb) Basal cell Dividing stem cell Olfactory neuron Olfactory knob Olfactory cilia Odorants Cribriform plate Bowman s gland Mature receptor cell Supporting cell Mucus Olfactory epithelium Airborne odors Each olfactory neuron expresses only one functional OR gene; (One neuron-one receptor rule) 12 (From Neuroscience) The screen versions of these slides have full details of copyright and acknowledgements 4

5 OR genes are also expressed in testis sperm chemotaxis ORs are G-protein coupled receptors (GPCRs) ORs contain seven transmembr ane α-helical regions OR genes do not have any introns in their coding regions (From Neuroscience) 13 The olfactory system uses combinatorial coding one OR recognizes multiple odorants and one odorant is recognized by multiple ORs, but different odorants are recognized by different combination of ORs Stimulus molecules Cells (From Malnic et al., 1999) 14 OR genes in humans 15 The screen versions of these slides have full details of copyright and acknowledgements 5

6 OR genes in the human genome 802 OR genes 388 functional genes Intact coding region (Met ~ stop codon) 414 pseudogenes (52%) Interrupting stop codons, frameshift mutations, long deletions 16 Distribution of OR genes in human chromosomes OR genes are present as genomic clusters They are located in all chromosomes except 20 and Y ~ 44% of all OR genes are in chromosome Cluster * : pseudogene Ψ : pseudogene Recently diverged genes are located closely to one another; 18 These genes were generated by repeated tandem gene duplications; The screen versions of these slides have full details of copyright and acknowledgements 6

7 Phylogenetic tree of 388 human functional OR genes Major Gene Families in Humans 19 (1) Evolutionarily closely related genes form tandem arrays However, (2) One genomic cluster often contains OR genes belonging to different phylogenetic clades that are distantly related (3) OR genes belonging to one phylogenetic clade are often found in several different genomic clusters (2) & (3) Several chromosomal rearrangements have occurred at the regions of OR gene clusters and the OR genes contained in different genomic clusters were shuffled. 20 Comparison of OR genes between humans and mice 21 The screen versions of these slides have full details of copyright and acknowledgements 7

8 Human Mouse Total no. of OR genes 802 1,391 No. of functional genes 388 1,037 No. of pseudogenes % pseudogene 52% 25% 22 Gene order and transcriptional orientations of orthologous genes are generally well conserved between humans and mice; The gene arrangement of OR gene clusters did not substantially change from the most recent common ancestor (MRCA) to the present humans or mice 23 There are a few cases in which the organization of OR genes is quite different between the two species; Translocation of chromosomes occurred in the mouse lineage; Orthologous relationships of OR genes between humans and mice are often one-to- multiple or multiple-to- multiple rather than one-to-one; Human or mouse genes were frequentl y duplicated after the separation of the two species; 24 The screen versions of these slides have full details of copyright and acknowledgements 8

9 The number of OR genes cluster in a mouse cluster is usually larger than that in the corresponding human cluster; The difference in OR gene numbers between the two species was generated primarily by tandem gene duplications within each genomic cluster; 25 Why do humans have a smaller number of functional OR genes and a larger fraction of pseudogenes than mice? Humans are vision-oriented animals, and the demand for olfaction is less strong than in mice; The olfactor y epithelium in primates is proportionatel y smaller than that in most of other mammals; The increase in the fraction of pseudog enes coincides with the acquisition of full trichromatic vision; (Gilad et al., 2004) The proportion of OR pseudogenes was estimated in 19 primate species by surveying 100 OR genes randomly chosen from each species; Catarrhines (humans, apes, and Old World monkeys) and the howler monkey showed a significantly higher proportion of OR pseudogenes than other New World monkeys and prosimians; 26 Why do humans have a smaller number of functional OR genes and a larger fraction of pseudogenes than mice? (1) The number of OR genes have decreased in the human lineage; (2) The number of OR genes have increased in the mouse lineage; How much is the contribution of the processes (1) and (2) to generating the difference in the OR gene repertoire between humans and mice? 388 functional genes 414 pseudogenes (52%) 1,037 functional genes 354 pseudogenes (25%) How many functional OR genes were there in the most recent common ancestor (MRCA) between humans and mice? 27 The screen versions of these slides have full details of copyright and acknowledgements 9

10 Number of gene duplications in the human or mouse lineage after the human-mouse divergence M1 M2 M3 H1 H2 H3 M4 M5 M6 M7 H4 M8 M9 M10 Human-mouse divergence Major Gene Families in Humans +? +? Human Mouse H1 ~ H4 Human genes M1 ~ M10 Mouse genes Human-mouse divergence 2 gene duplications in the human lineage 4 gene duplications in the mouse lineage 28 Phylogenetic tree of 388 human and 1,037 mouse functional OR genes The human lineage acquired ~ 60 new OR genes The mouse lineage acquired ~ 350 new OR genes + 60 Human +350 Mouse 29 How many functional genes in the MRCA were inactivated in the human or mouse lineage after the human-mouse divergence? -? Human -? Mouse Is the closest functional gene to a given human pseudogene a human gene or a mouse gene? HΨ: human pseudogene HΨ M HΨ H The MRCA gene was inactivated in the human lineage; HΨ H M The MRCA gene generated both functional genes and pseudog enes; 30 The screen versions of these slides have full details of copyright and acknowledgements 10

11 The human lineage lost ~ 430 functional OR genes in the MRCA; The mouse lineage lost ~ 60 functional OR genes in the MRCA; functional genes 414 pseudogenes (52%) 1,037 functional genes 354 pseudogenes (25%) ~ 750 functional genes The number of functional genes in the MRCA was estimated to be ~ 750, which is close to the mean of the number s of functional genes in current humans and mice; The gene loss in the human lineage and the gene gain in the mouse lineage have nearly equally contributed to the generation of the difference in the number of OR genes between the two species; 31 Evolution of OR genes in vertebrates 32 OR genes are present in vertebr ate species; Several OR genes were identified from lampreys; Vertebrate phylog en y Lamprey Jawless vertebrates Hagfish Lamprey Cartilaginous fishes (sharks, rays) Ray-finned fishes Coelacanth Jawed vertebrates Lungfish Tetrapods (amphibians, reptiles, birds, mammals) Fishes have a much smaller number of OR genes (~ 100) and recognize water-soluble odorants such as amino acids, bile acids, sex steroids, and prostaglandins; Insects also have genes named odorant receptors or ORs ; Functionall y similar to vertebr ate ORs GPCRs No sequence similarity to vertebrate OR genes Contain introns unlike vertebr ate OR genes 33 The screen versions of these slides have full details of copyright and acknowledgements 11

12 Number of OR genes in six species Major Gene Families in Humans Total Functional genes* Pseudogenes or partial sequences Zebrafish Pufferfish W estern clawed frog Chicken Mouse 1,391 1, Human * These numbers represent lower bounds, because the draft genome sequences for some species are incomplete; 34 Phylogenetic tree of 1,026 functional OR genes from five species Class I (α) Class II (γ) Human class II genes form a monophyl eti c clade with most (~ 90%) of the genes from frogs and chickens; To reduce the size of the tree, a phylogenetic tree containing all non-group γ genes and four representative group γ genes was constructed; 35 Condensed tree (70% level) for 310 OR genes > 90% bootstrap value > 80% bootstrap value α β γ δ ε ζ Lamp -rey η θ κ Outgroup Type 1 Type 2 Vertebrate Two non-or genes GPCR can genes be classified were used into two as the groups, outgroup; type 1 and type 2; (adenosine The divergence A1 receptor, between α2b-adrenergic type 1 and type 2 receptor) genes predates the divergence between jawed vertebrates and jawless vertebrates; The Phylogenetic MRCA between relationships fishes and with tetrapods > 70% had bootstrap at least nine supports ancestral are OR shown; genes and all OR genes identified were classified into nine groups (α ~ κ) each The of branch which lengths originated do from not one reflect ancestral their evolutionar gene; y distances; 36 The screen versions of these slides have full details of copyright and acknowledgements 12

13 Number of functional OR genes in different groups Major Gene Families in Humans Ligand α Airborne β ? Type 1 γ δ Airborne Water-soluble ε Water-soluble ζ Water-soluble Type 2 η θ ? κ >1? 0 Total ?? Water-soluble > 80% 5-80% 0-5% 37 Evolutionary dynamics of vertebrate OR genes ~450 million years ago MRCA between jawed and jawless vertebrates 2 genes (type 1 & type 2) ~400 million years ago MRCA between fishes and tetrapods 9 genes (Groups α ~ κ) Terrestrial adaptation Expansion of group γ genes Loss of OR genes specific to water-soluble odorants Present Fishes Amphibians Birds / Mammals 38 Summary The variation in OR gene repertoire among vertebrate species is largely caused by environmental factors; In the tetrapod lineage, repeated gene duplicati ons and massive gene losses appear to have occurred in the process of adaptation to terrestrial environments; In the fish lineage, the change in OR gene repertoire seems to be small, probably because the environmental change has been small; The number of OR appears to be controlled by random factors consider ably; Each species has a large number of pseudogenes; The OR gene family is subject to an extreme form of birth-and-death evolution 39 The screen versions of these slides have full details of copyright and acknowledgements 13

14 Other chemosensory receptor genes 40 Receptors for chemosensation Olfactory receptors (ORs) Odors Vomeronasal receptors (V1R, V2R) Pheromones (+ odors) Taste receptors (T1R, T2R) Tastes (Mombaerts, 2004) OR (Intronless) V1R, T2R (Intronless) V2R, T1R (Multiple exons, long N-terminal tail) All of these family genes are GPCRs ORs, V1Rs, and V2Rs are evoluti onaril y unrelated and show no significant sequence similarities to one another T1Rs are similar to V2Rs and T2Rs are similar to V1Rs 41 Vomeronasal receptors Main olfactory bulb Accessory olfactory bulb Main olfactory epithelium Vomeronasal organ (Firestein, 2001) Vomeronasal receptors are expressed in vomeronasal organ (VNO) Pheromone perception Vomeronasal and olfactory system have some overlapping functions The VNO is vestigial in human adults; Although the VNO develops in the human fetus, it degenerates before birth There are a few intact V1R genes, > 100 V1R pseudogenes, and no V2R genes in the human genome TPR2, which is essential for VNO function in mice, is a pseudogene in humans, apes, and Old World monkeys Mice and rats have > 100 functional V1R genes and > 50 V2R genes VNOs do not exist in fishes; Fishes have many V2R genes, but they are expressed in the olfactory epithelium 42 The screen versions of these slides have full details of copyright and acknowledgements 14

15 Taste receptors Five modalities of tastes: Bitter T2Rs Sweet, sour, bitter, salty, umami Sweet and umami T1Rs Sweet: The taste of L-glutamate Deliciousness Discovered by Kikunae Ikeda in 1909 Kikunae Ikeda Courtesy of Ajinomoto Co., Inc. Salty and sour ion channels T1R2 + T1R3 Umami: T1R1 + T1R3 43 Number of chemosensory receptor genes in vertebrates Zebrafish Pufferfish Frog Chicken Opossum Cow Dog Rat Mouse Human OR 98 (35) 44 (54) 410 (478) 78 (476)?? 872 (222) 1,201 (292) 1,037 (354) 388 (414) V1R 2 (0) 1 (0) 21 (2) 0 (0) 98 (30) 40 (45) 8 (33) 106 (66) 187 (121) 5 (115) V2R 44 (8) 18 (29) 249 (448) 0 (0) 79 (72) 0 (8) 0 (5) 59 (109) 70 (139) 0 (7) T1R ? T2R 4 (0) 6 (0) 49 (12) 3 (0) 26 (5) 12 (15) 15 (5) Number of pseudogenes are shown in parentheses 37 (5) 35 (6) 25 (11) 44 Conclusions 1. The size of the OR gene family is considerably different between humans and mice; The difference is apparently caused by massive inactivation of OR genes in the human lineage and a substantial increase of OR genes by repeated gene duplications in the mouse lineage 2. The OR gene family in fishes is much smaller but much more divergent than that in mammals; The mammalian OR gene family is characterized by the loss of many group genes that existed in the ancestor of vertebrates and the subsequent expansion of specific groups of genes 3. Vertebrate OR multigene family changed dynamically depending on the evolutionary lineage and are subject to extreme form of birth-and-death evolution 4. Some of the other chemosensory receptor gene families showed an evolutionary pattern similar to that of OR genes 5. It appears that the number and the types of genes in chemosensory receptor gene families have evolved in response to environmental needs, but they are also affected by fortuitous factors 45 The screen versions of these slides have full details of copyright and acknowledgements 15

16 Thank you! The screen versions of these slides have full details of copyright and acknowledgements 16

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