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The evolution of sex chromosomes: similarities and differences between plants and animals

Silene dioica male. Silene latifolia female. The evolution of sex chromosomes: similarities and differences between plants and animals. Deborah Charlesworth Institute of Evolutionary Biology, University of Edinburgh. Papaya female. 1. WHAT are sex chromosomes?

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The evolution of sex chromosomes: similarities and differences between plants and animals

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  1. Silene dioica male Silene latifolia female The evolution of sex chromosomes: similarities and differences between plants and animals Deborah Charlesworth Institute of Evolutionary Biology, University of Edinburgh Papaya female

  2. 1. WHAT are sex chromosomes? • and what are NOT sex chromosomes • 2. WHY do sex chromosomes evolve loss of recombination? • 3. WHEN did sex chromosomes of some important species evolve? • and when did recombination stop? • and 4. HOW did recombination stop? • 5. WHERE are the sex-determining loci in relation to the regions where recombination is absent? • 6. WHAT are the consequences for sex chromosomes of stopping recombination?

  3. Sex chromosomes have been known to geneticists for a long time • Muller (1914): reviewed evidence for X-Y pairing (indicating their homology) and Y genetic degeneration (suggested by C.W. Metz) and discussed recessive loss of function mutations as the cause of degeneration • Haldane (1922, p. 107): “If sex were determined by a single factor, it is very difficult to see what advantage there could be in its being linked with other factors)” • An excellent review of the classical work is JJ Bull’s 1983 book “Evolution of Sex Determining Mechanisms” but many important things have only become clear very recently, and great progress is occurring • Lahn and Page (1999): human genome sequence reveals sequences of genes shared between X and Y, often highly diverged. Carvalho (2001): Drosophila Y-linked genes • Recent data are starting to help us understand why and how recombination gets stopped between the X and Y (and what the consequences are) • Further evolutionary changes of sex chromosomes can now be studied in detail

  4. X Y Classical sex chromosomes Humans Y is ~ 1/3 of the size of the X X ~ 1,098 genes Y 24 genes Male-specific Y region MSY without recombination Pseudo-autosomal region PAR In Drosophila, the Y is about the same size as the X, but the X has several thousand genes, while the Y has around 20. No X gene has a Y homologue.

  5. Some species, including many plants have small sex-determining regions Several plant ‘sex chromosomes’ have the sex-determining genes located within a small region (blue; only 10% of chromosome 1 of papaya) where recombination does not occur (Liu et al. 2004) • Some fish sex chromosomes may be similar • Does small size mean young, or primitive? Otherplants have heteromorphic sex chromosomes like those of humans and Drosophila, or neo-sex chromosomes Liu et al. 2004. Nature 427:348-352 neo-sex chromosomes also occur in plants

  6. PAR Silene latifolia MSY region Y X Some highly heteromorphic plant sex chromosomes The liverwort, Marchantia polymorpha (haploid) X Yamato et al. (2007) Proc. Natl. Acad. Sci. USA 104, 6472-6477 Y

  7. Meiosis 2n → n Haploidsex chromosomes in a bryophyte with separate sexes (Ceratodon purpureus) Diploid sporophyte XY AA NOTE No XX Genetic map showing 15 linkage groups, including the XY chromosome pair (121 AFLP, 3 genic markers ) Fertilization n → 2n Haploid Y A Male gametophyte X A Female gametophyte McDaniel et al. 2007 Genetics 176:2489-2500

  8. Chromosome(s) transmitted to female progeny X1 neo-X or X2 Chromosome(s) transmitted to male progeny Neo-sex chromosomes due to Fusions/translocations X Autosome Y Y-autosome fusion X-autosome fusion neo-X Y1 neo-Y or Y2 neo-Y In Drosophila, there is no recombination in males Thus, both kinds of fusion create non-recombining neo-sex chromosomes Chromosome fusions can lead to heteromorphism Fusion can also occur in X0 systems

  9. Neosex chromosomes in the genus Drosophila Complete degeneration of the ancestral Y Carvalho, A. B., and A. G. Clark. 2005. Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307:108-110.

  10. Neo-sex chromosomes occur in many species Rowell, D. (1985). Complex sex-linked fusion heterozygosity in the Australian huntsman spider Delena cancerides (Araneae: Sparassidae). Chromosoma93, 169-176. RENS et al., 2004 PNAS 101: 16257-16261 GRÜZNER et al., 2004 Nature 432: 913-917.

  11. X Y marsupial X autosome in marsupials • The mammalian sex chromosomes evolved via a fusion since the split from marsupials • The Y can be lost entirely if genes required for male fertility can move to a different chromosome • Some species have X/0 male genotype, but males are still fertile, e.g. Drosophila affinis • In D. pseudoobscura,the X chromosome has been fused to an autosome, and the Y has lost all male fertility genes • So, even if the Y chromosome degenerates, we do not need to worry about a future without males • Clearly, the Y cannot be lost unless the sex-determination function is replaced by a new gene (or the Y gene moves to another chromosome) • Such changes are theoretically possible: e.g. DOORN and KIRKPATRICK, 2007 Turnover of sex chromosomes induced by sexual conflict. Nature 449: 909-912, KOZIELSKA et al., 2010 Segregation distortion and the evolution of sex-determining mechanisms. Heredity104, 100-112.

  12. Changes can occur from XY to ZW system (even in different populations of the same species) An example of the use of genes to demonstrate that the XY pair of chromosomes changed into a ZW pair Uno et al. 2008. Comparative chromosome mapping of sex-linked genes and identification of sex chromosomal rearrangements in the Japanese wrinkled frog (Rana rugosa, Ranidae) with ZW and XY sex chromosome systems. Chromosome Research:1217-7

  13. Summary of diversity of sex-determining chromosomes • CLASSICAL • Non-recombining over a large genome region, with small “pseudo-autosomal region(s)”, e.g. mammal and Drosophila X and Y, bird and Lepidopteran Z and W • Genetically degenerated • loss of genes relative to the X (or lower function — see later) • The Y can sometimes be totally lost (X0 systems) • Y is enriched in male-function genes, and is rearranged relative to the X • “LOCAL SEX-DETERMINING REGION” • Chromosome is largely pseudo-autosomal • The same properties as classical sex chromosomes, in a restricted region of genome • We know much less about these, and modern molecular approaches are helping get information • HAPLOID • Haploid male genotype is Y and female is X • NOT SEX CHROMOSOMES • single-gene systems, e.g. sex-determination factor that replaced a previous one, honeybee complementary sex-determiner • plant, fungal and algal incompatibility regions (but have some similar properties)

  14. Silene vulgaris Hermaphrodite Female Monoecious Hermaphrodite Environmental sex-determination Mutation to loss of ♂ or ♀specific developmental pathway ♂-sterility mutation Genetically + environmentally determined unisexuals Gynodioecious (♀and hermaphrodite) ♀-sterility mutation GSD dioecy (♂ and ♀) X Y Proto-sex chromosomes Non-recombining region Replacement by new sex-determining gene Translocation onto another chromosome Mutation to sexually antagonistic gene New non-recombining region evolves

  15. Possible origins of sex-determining chromosomes

  16. 2. WHY does recombination stop on sex chromosomes? • Haldane (1922, p. 107): “If sex were determined by a single factor, it is very difficult to see what advantage there could be in its being linked with other factors)” (Sex ratio and unisexual sterility in hybrid animals. J. Genetics 12:101-109) • Nei (1969, 1970): models for lack of recombination and consequent accumulation of detrimental mutations leading to degeneration • Nei, M. 1969. Linkage modification and sex difference in recombination. Genetics 63:681-699; 1970. Accumulation of nonfunctional genes on sheltered chromosomes. American Naturalist 104:311-322. • But many modern authors are much less clear e.g. “heteromorphic sex chromosomes have evolved ….when one autosome develops a dominant sex-determining mutation” • Itoh et al. 2007. Molecular cloning of zebra finch W chromosome repetitive sequences: evolution of the avian W chromosome. Chromosoma 117:111-121.

  17. 1. Loss of stamen promoting factor (SPF or M) creates females 2. Gynoecium suppressing factor (GSF or SuFemale) reduces female functions Why are 2 genes involved? In many plants,males and females are simply hermaphrodites with parts missing. In S. latifolia, sex-determination is genetically simple. Mutants support the hypothesis that at least 2 genes are involved Hermaphrodite Picture from Shigeyuki Kawano Neuter

  18. 1 2 The simple 2 gene evolutionary model suggests that (1) sex determining loci must initially be linked for separate sexes to evolve and (2) once females are present, hermaphrodites are selected to re-allocate more to male and less to female functions M SuFemale “proto-Y” “proto-X” m f Selection should then act to reduce recombination between the initial 2 genes slightly older proto-Y, with MSY region M2 M SuFemale

  19. Summary of question 2: There is no selection to reduce recombination unless at least 2 genes interact • Qvarnstrom & Bailey. 2009. Heredity 102:4-15 are completely wrong! • The evolution of identifiable heteromorphic sex chromosomes is initiated by the spread of a sex-determining gene. This occurs when a new mutation at a locus leads all its carriers to become the same (subsequently heterogametic) sex, with the chromosome carrying this mutation becoming the Y/W chromosome. In eutherian mammals, for example, the development of males is controlled by the SRY gene found only on the Y chromosome • Here is another misunderstanding (Sekido & Lovell-Badge. 2009. Tr. Genet. 25:19-29) • In eutheria, Sox3 is X linked and involved in the development of the CNS, the pituitary, pharyngeal region and is perhaps involved in male fertility, but it has no demonstrable role in sex determination. The original mutation that led to the origin of Sry, therefore, seems to have involved the acquisition of a novel function (neomorph) and it could have been the primary drive for the separation of the two sex chromosomes. • These authors are confused between the evolution of sex chromosomes and the evolution of modified sex-determining systems • To understand why the sex chromosomes don’t recombine, we need to understand WHY interacting genes are involved, which requires understanding HOW separate sexes evolved, and what kinds of genes were involved • BC, DC (1978, Amer. Nat. 112:975-997) : evolution of sex-determining region with two loci (driving selection for less recombination) • This question is separate from: how is recombination lost? • single step when the sex chromosomes orginated or a gradual process, with several successive steps, and whether inversions were involved?

  20. How can one get sex-linked genes to map sex-determining chromosomes? • To estimate ages of sex chromosomes, and to study degeneration, we need to find genes and studyalignableX and Y alleles • There are few known mutant phenotypes (as Muller realised) • Molecular methods are needed (Muller realised this too, in 1922) • Even with “complete” genome sequences of important “model organisms” there are still great difficulties • The gene content of the Y chromosomes of important “model organisms” have only recently been determined • Drosophila: Carvalho et al. 2001 PNAS 98:13225-13230 • Humans: SKALETSKYet al., 2003 Nature 423: 825 - 837, BHOWMICK et al, 2007 Genome Res. 17: 441-450; Chimpanzee: HUGHES et al. 2010 Nature (13 January 2010). The mouse Y is still not well characterized • and sex chromosomes of non-model organisms” are only now starting to be studied — EST sequences can be very helpful • e.g. Dreyer et al. 2007. ESTs and EST-linked polymorphisms for genetic mapping and phylogenetic reconstruction in the guppy, Poecilia reticulata. BMC GENOMICS 8:269, Tripathi et al. 2009 Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation. Proceedings of the Royal Society B276, 2195-2208. How can one get sex-linked genes to map sex-determining chromosomes?

  21. Why is it difficult to sequence Y chromosomes? • Low gene densitymakes finding genes very difficult. • Rearrangements: one homolog cannot used to help align the other, unlike the autosomes • Y can be sequenced from a single individual • Their intergenic regions and introns contain large amounts of repetitive sequence, so it is difficult to find the different parts of the same gene • Assembly of highly repetitive genomes is very difficult • it requires large sequenced regions, such as BAC clones, but these may be difficult to sequence if they contain repetitive sequences • These are sometimes unstable when cloned, and so cannot be sequenced • They may compete in PCR reactions, so that some copies fail to amplify • If the repetitive sequences are AT-rich, poor strand separation may impede sequencing reactions • In humans and Drosophila, Y-linked genes have been found, and, in humans, some have X-linked alleles

  22. Genes on Y only Genes on X and Y The human MSY region genes Heterochromatin Y genes with male functions can be kept on the Y because the sex chromosomes don’t recombine across much of their length. These genes are probably prevented from degenerating There are a few X-Y gene pairs (X homologous genes), even in the non-recombining regions (NRY) Many Human Y genes have male functions

  23. Maybe one should sequence the genome? Overview of the Marchantia polymorpha YR2 region — so far in this species mainly Y chromosome data, not X and Y. This species is expected to have an old Y chromosome 50 Y-linked housekeeping genes are also found in females (presumably non-degenerated genes, with autosomal or X-linked copies) 14 Y-linked genes are unique to males, and expressed only in reproductive organs G = genes (indicated by arrows ) P = pseudogenes O= organelle sequence T = transposable element

  24. The genus Silene Dioecious (independent evolution) Gynodioecious Dioecious Hermaphrodite I emphasized how helpful it is to identify genes, not just anonymous markers or sequences, and that plants are interesting for studying de novo evolution of sex chromosomes (because sex chromosomes have evolved recently in several taxa) Plants BUT findingX and Y genes in non-model species is difficult, and the S. latifolia genome is big! Estimated from ITS sequences by Desfeux, C., et al. 1996. Proc. Roy. Soc. Lond. B. 263:409-414 Recent work with more nuclear genes supports these phylogenetic relationships Humans

  25. How else can one find sex-linked loci? • Testing linkage of known genes involved in flower development, using families • MROS3-X and -Y (Dave Guttman, 1998) • SlAp3 (Sachi Matsunaga 2003) • cDNA probing of micro-dissected Y chromosomes • SlX/Y1 (Delichère et al. , 1999) • SlX/Y4 (Atanassov et al., 2001) • SlX/Y3 (Nicolas et al. 2005 • Genes can now be discovered from cDNA libraries and EST sequences of any species of interest • SlSs-X/Y Dmitry Filatov • SlCyp-X/Y Roberta Bergero Isomerase, cyclophilin type • Sl8-Y only Roberta Bergero Mono-oxygenase/haem binding protein • Sl6a and b X/Y Roberta Bergero Unknown protein (2 Y and X copies) • Sl7X/Y Roberta Bergero Unknown protein • RB11 and RB18 Roberta and Vera Kaiser • Differential display • DD44 (Moore et al., 2003) • It is interesting to combine sequence divergence estimates with genetic maps

  26. X- and Y-linkage for locus Sl6 EST sequences were used to obtain sequences Intron positions of genes at low copy number were determined from the Arabidopsis thaliana and rice genomes PCR primers were designed to cross introns to find length variants to do genetics F1 progeny Parents Y-linked 1830 bp 730 bp maternal X 2072 bp 700 bp 590 bp paternal X 500 bp 510 bp maternal X 590 bp paternal X

  27. FAM FAM FAM FAM FAM Roberta’s ISVS method Forward primer Intron region Exon A Exon B Reverse primer Incorporation of labeled universal primer after the first PCR cycles Analysis by capillary electrophoresis For product sizes > 450-500 bp, digest with restriction enzyme MboI HaeIII MboI MboI HaeIII

  28. Evidence for X/Y linkage of the SlCyp gene Intron 3 variants, showing Y-linkage of 438 bp band Intron 2 variants , showing X-linkage of 259 and 260 bp bands 2 male and 2 female F1 plants Parents 260Xm 257Y 260Xm 259Xp 259Xp 260Xm 257Y 438 bp in males only 447 bp 447 bp

  29. 3. WHEN did sex chromosome systems evolve, and when did recombination stop? • Some classical sex chromosomes are probably old • We don’t yet know how long it takes for the full set of features to evolve • It is often assumed that all other systems are young • but we need data. It is now possible to get evidence, using DNA sequences, estimating divergence between homologous X and Y sequences, and assuming a molecular clock • heteromorphism can evolve rapidly, e.g. by chromosome fusions • For most species, it is difficult to get the genes for such studies

  30. (1) Mostly old part of X (all but 2 genes present in marsupial X chromosomes) (2) Few genes on the X are still detectable on the Y Stratum 1 (3) In contrast with Xq, many Xp genes still have detectable homologues on the Y X-Y divergence, Ks Autosomal in marsupials (added to X and Y by transposition. Stratum 3 Strata 4 & 5 Stratum 2 2 genes transposed very recently to the Y Xp Xq recent transposition PAR1 X-Y divergence in humans LAHN & PAGE, 1999 Four evolutionary strata on the human X chromosome. Science 286: 964-967. SKALETSKY et al. 2003. Nature 423:825 - 837.

  31. Autosomal in marsupials (added to X and Y by transposition) Mostly old part of X (all but 2 genes present in marsupial X chromosomes) Strata are found in organisms other than humans (Z versus W) (X versus Y) Human (X versus Y) (X versus Y) NOTE the different y axis scale PAR PAR PAR1 transposition inversion Lawson-Handley et al., 2004 Genetics 167: 367-376Nam & Ellegren. 2008. Genetics 180: 1131 - 1136 Bergero et al., 2007 Genetics 175: 1945-1954

  32. Phylogenetic analysis of bird Z and W chromosomes also suggests that recombination between them stopped at different times from LAWSON-HANDLEY et al., 2004 Genetics 167: 367-376 Pseudo- autosomal end Chicken Z Genes that stopped recombining after split of taxa Genes in region where Z- W recombination stopped before split of major bird taxa Some bird taxa probably have small sex-determining regions

  33. Giemsa C-bands G-bands Painting with Locations of staining by BrdU chicken Z markers probe Z W Non-recombining region has probably remained small Ostrich Large non-recombining region Chicken Markers: Gradual evolution of bird sex chromosomes is also evident when different taxa are compared — some taxa have not undergone all the steps that others have taken Z chromosomes of both taxa share several markers Thus they probably had the same ancestral sex chromosome Recombination has been suppressed only in the chicken lineage (including other neognathae), and not in palaeognathous birds Nishida-Umehara et al. 2007 Chromosome Research 15:721-734 Nanda, I et al.. 2008. Cytogenet Genome Res 122:150-156.

  34. Gradual evolution of snake sex chromosomes P. molurus (Pythonidae) Females are WZ E. quadrivirgata (Colubridae) Matsubara et al. (2006) PNAS 103: 18190 Many (11/11) genes shared between Z and W (small sex-determining region) 3/11 genes shared between Z and W No genes shared between Z and W (W has lost most genes) T. flavoviridis (Viperidae)

  35. Ks values in 6 X and Y Marchantia polymorphagenes suggest that thissex chromosome system is old (Ks isuncorrected synonymous or silent site divergence) Ks • If we had a good molecular clock, we could translate Ks values into times when X-Y recombination stopped • It is not yet possible to tell whether there are strata in this plant, or if the Y and/or X is degenerated

  36. Is papaya (with a small MSY) a young system? Divergence is low between papaya X and Y gene sequences Ks values in 4 papaya genes from a BAC clone X and Y from hermaphrodite (Yh,YU et al, 2007 Plant Journal 53: 124-132) X and Y from male (YU et al, 2008 Tropical Plant Biology 1: 49-57) It is not yet possible to tell whether there are strata in this plant, because only 2 BACs were sequenced (< 150 kb, whereas the size of the MSY is ~ 10 Mb)

  37. Summary of question 3 • Some classical sex chromosomes are old • Even in such old sex chromosomes, recombination in most of the chromosome sometimes continued for long after the sex chromosome first evolved, and, in some species (but not all) later stopped in some regions • in mammals, birds and Silene latifolia • It is not yet clear whether species with small non-recombining regions of their sex-determining chromosomes are always young sex chromosomes • Some of them could be sex-determining chromosomes with single gene control of gender, and therefore without selection for reducing recombination

  38. M SuFemale “proto-Y” “proto-X” m f M2 M SuFemale “proto-Y” “Y” WHY are there strata? Why doesn’t recombination just stop across the entire sex chromosome?The simplest 2 gene evolutionary model above suggested that sex determining loci must initially be linked for separate sexes to evolve 1 2 3 Other genes may be added to the system in a 3rd step (and so on) Reduced recombination between initial 2 genes sexually antagonistic male-enhancer

  39. The hypothesis of sexually antagonistic male-enhancers is plausible, but all evidence to date is indirect, and the only such genes yet identified are in the guppy • indeed many are wholly or partially sex-linked • without sexual antagonism, there should be no selective pressure converting hermaphrodites into males (the female functions of hermaphrodites could be maintained unchanged while male functions improve). • There may be molecular ways to test for antagonistic genes • in chicken and mouse, Mank et al. (2008American Naturalist 171:35-43) searched for genes with different male and female expression patterns • many of these will NOT have antagonistic effects (they could just have sex-specific expression), but the set of such genes should include genes with antagonistic effects • They found that this set of are less likely to be expressed in multiple tissues (with the potential for conflicting selection pressures) than the genome average, even after excluding sex-linked genes; however, a difference in tissue-specificity could be explained without sexually antagonistic effects

  40. Fertility of female offspring High fertility female parents Low fertility female parents Fertility of male offspring Low fertility female parents High fertility female parents Low High Fertility of male parents • Drosophila experiments that allowed selection in males only show that female fitness indeed declines • This is consistent with a trade-off between the sex functions, but it could be due just to stopping selection in females • Reversal in quality of progeny, depending on whether they had high or low fertility parents, is clear evidence for trade-offs, but it does not prove intra-locus sexual conflict Pischedda & Chippindale (2006, PLoS Biology 4:e356)

  41. The best evidence so far for sexually antagonistic male-enhancers is in the guppy fish, Poecilia reticulata • Guppy males are highly polymorphic for color patterns and their genetics has been studied analysis since 1927 • This fish has 23 pairs of chromosomes — 22 autosomal and one sex-determining. Males are heterogametic (the sex determination mechanism is “XX/XY”, and the “YY” genotype is viable) • Almost all the genes determining guppy colour patterns (except for body color) are fully or partially sex-linked or sex limited (unlike what is found in other teleosts) • Winge, O. 1927. The location of eighteen genes in Lebistes reticulatus. Journal of Genetics 18,. A peculiar mode of inheritance and its cytological explanation. Journal of Genetics 12:137. • With the possibility of using naturally occurring polymorphic sequence variants as genetic markers, it is now possible to make a more detailed genetic linkage map and find out if the Y has an excess of male attractiveness factors • Molecular markers have now been found on the Y chromosome, closely (but none fully) linked to the sex-determining region. • Shen et al (2007, Aquaculture 271:178-187), TRIPATHI et al. (2009, Proc. Royal Society B 276: 2195-2208) • Overall, the results suggest that the non-recombining MSY region may not be very large, and that the colour variants may be controlled by polymorphic genes in the PAR

  42. 4. HOW did recombination stop, how do MSY regions expand? Lahn & Page’s suggested evolutionary history of the mammalian sex-chromosomes • ‘..there is little evidence demonstrating the importance of [chromosome rearrangements versus genes modifying recombination] in the evolution of X-Y crossover suppression’ (Bull 1983) • There are many inversions on the mammalian Y BUT the known inversions on the Y occurred relatively recently, and these cannot be involved in stopping recombination (since, in most of the Y, it stopped long ago) SRY/ SOX3 Translocation

  43. X chromosomes NRY regions Mammalian X chromosome gene arrangements are stable, while Y chromosomes are highly rearrangedBUT inversions occurred since humans split from chimpanzeesandmodifier genes can also change recombination rates during evolution PAR1(orPSA) recently transposed from the X Yp degenerated copies of X genes Heterochromatic region “Ampliconic” (duplications) Human degenerated X genes inverted PSA2 Yq inverted Chimpanzee

  44. The papaya MSY (male-specific non-recombining) regions have been rearranged, even in just the two BACs so far studied • It is not known whether this region contains the sex-determining genes, or whether these inversions caused recombination to stop, but this region is only a small part of the MSY • The rearrangement in this region is shared by the Y and Yh, and differentiates both of them from the X • Thus it either dates from, or pre-dates, the evolution of hermaphrodites, suggesting that several events suppressing recombination have occurred X from hermaphrodite Y from hermaphrodite (Yh) 6.5 Mb Y from male Y from hermaphrodite (Yh) 6.5 Mb X from male X from hermaphrodite • X-Y divergence • (%) 13 - 19 2 - 4 10 - 13 Yu et al. 2008. Tropical Plant Biology 1: 49-57

  45. The most recent strata in the human MSY already have several inversions • Stratum 5 may involve an inversion, but stratum 4 includes several inversions ( ) • Rearrangements may thus occur as a consequence of lack of recombination, as well as causing recombination to cease (Lemaitre et al. 2009 Footprints of Inversions at Present and Past Pseudoautosomal Boundaries in Human Sex Chromosomes. Gen Biol Evol.1, 56 - 66) Stratum 4 Stratum 3 Stratum 5 PAR1 Ross et al. 2005. Nature 434:325-337

  46. 5. Where are the sex-determining genes? Did X-Y recombination stop in S. latifolia due to inversions?Y chromosome deletion map of the Y, based on 3 parental plants A C B In one parent plant, the Y chromosomes gene SlY1 is in a different location In two parent plants the Y chromosomes gene SlY6b is absent

  47. Pseudo-autosomal Present X gene order Alternative Y gene order Proto-Y1 Present Y Possible rearrangements in the Y, relative to the X p arm RB11 (no Y copy) RB18X M m M RB18Y Suf SuFemale SuFemale q arm Paracentric inversion Pericentric inversion These results show that inversions happened after X-Y recombination first stopped in the region containing genes SlXY3, 4, 7 and 6a

  48. Accumulation of transposable element on Y chromosomes may promote rearrangements • Loss of a gene in primates: Nakayama & Ishida. 2006 Genome Res. 16:485-490. • Rearrangements can obscure X-Y heteromorphism • Gene conversion between paralogs in the human Y: Bosch et al. 2004. Genome Res. 14:835-844. Cytogenetic maps of the threespine stickleback X and Y chromosomes, based on FISH with genes X Y inversion X Y Heteromorphic X-Y pair X Y deletion of part of Y deletion inversion on Y and/or insertion, making heteromorphism hard to detect Ross and Peichel. Genetics 2008;179:2173-2182

  49. 6. Why does stopping recombination lead to sex chromosome degeneration, and how fast is it? • It has been known since 1918 that classical Y chromosomes are degenerated chromosomes • Muller, H. J. 1918. Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics 3:422-499. • “It is probably needless to point out that the W and especially the Y chromosome ….. show the expected evidences of …. degeneration and differentiation from their homologues, both genetically and cytologically. The evidences are now as follows: • X-linked mutations affecting visible phenotypes are manifested in XY males • therefore the Y does not carry alleles that can cover up mutations • Infrequent dominant Y (and W) linked mutations” • “Great variations in their own size and shape even in closely related species” • Synaptic attraction between them and their homologues • “but the sex chromosomes in the heterozygous sex tend to remain condensed during the growth period, while the autosomes are spinning out for intimate conjugation, and there is frequently delayed synapsis” • “also lack of crossing over between them and their homologues, even …. where other chromosomes are undergoing crossing over”

  50. Y chromosome degeneration • Loss of genes • Well illustrated by classical sex chromosomes • for example, the human X region that has been non-recombining longest has the lowest proportion of intact genes on the Y (at most, 5), whereas the probable number carried on the X chromosome is 734 (based on a count done by Gabriel Marais, using Ensembl version 47) • Worse gene function • amino acid substitutions that reduce functioning • less use of optimal codons • expression levels changed relative to X (presumably wrong levels) • Transposable element insertion is often included as an aspect of Y degeneration, and degeneration may indeed be caused partly by transposable element insertions, but we don’t actually know this • it is possible that these insertions are neutral • they could insert after genes or the sequences controlling their expression have degenerated

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