Dosage compensation evolution in plants: theories, controversies and mechanisms
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Review
PubMed
35306896
PubMed Central
PMC8935305
DOI
10.1098/rstb.2021.0222
Knihovny.cz E-resources
- Keywords
- Y degeneration, cis-regulatory sequence divergence, dosage balance, dosage-sensitive genes, imprinting, sex chromosomes,
- MeSH
- Dosage Compensation, Genetic * MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes * genetics MeSH
- Plants genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
In a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation (DC), a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species, we lack the data to differentiate between global and gene-by-gene DC. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.
CEFE University of Montpellier CNRS EPHE IRD Montpellier France
Departamento de Biologia Faculdade de Ciências Universidade do Porto 4099 002 Porto Portugal
Laboratoire 'Biométrie et Biologie Evolutive' CNRS Université Lyon 1 Lyon France
See more in PubMed
Charlesworth D, Charlesworth B, Marais G. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity (Edinb.) 95, 118-128. (10.1038/sj.hdy.6800697) PubMed DOI
Bachtrog D. 2013. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14, 113-124. (10.1038/nrg3366) PubMed DOI PMC
Charlesworth B. 1978. Model for evolution of Y chromosomes and dosage compensation. Proc. Natl Acad. Sci. USA 75, 5618-5622. (10.1073/pnas.75.11.5618) PubMed DOI PMC
Rice AM, McLysaght A. 2017. Dosage-sensitive genes in evolution and disease. BMC Biol. 15, 78. (10.1186/s12915-017-0418-y) PubMed DOI PMC
Lenormand T, Roze D. 2021. Y recombination arrest and degeneration in the absence of sexual dimorphism. Science 375, 663-666. (10.1101/2021.05.18.444606) PubMed DOI
Ercan S. 2015. Mechanisms of X chromosome dosage compensation. J. Genomics 3, 1-19. (10.7150/jgen.10404) PubMed DOI PMC
Marin R, et al. 2017. Convergent origination of a Drosophila-like dosage compensation mechanism in a reptile lineage. Genome Res. 27, 1974-1987. (10.1101/gr.223727.117) PubMed DOI PMC
Lucchesi JC, Kuroda MI. 2015. Dosage compensation in Drosophila. Cold Spring Harb. Perspect. Biol. 7, a019398. (10.1101/cshperspect.a019398) PubMed DOI PMC
Ohno S. 1967. Sex chromosomes and sex-linked genes. Berlin, Germany: Springer.
Loda A, Heard E. 2019. Xist RNA in action: past, present, and future. PLoS Genet. 15, e1008333. (10.1371/journal.pgen.1008333) PubMed DOI PMC
Xiong Y, Chen X, Chen Z, Wang X, Shi S, Wang X, Zhang J, He X. 2010. RNA sequencing shows no dosage compensation of the active X-chromosome. Nat. Genet. 42, 1043-1047. (10.1038/ng.711) PubMed DOI
Chen J, Wang M, He X, Yang JR, Chen X. 2020. The evolution of sex chromosome dosage compensation in animals. J. Genet. Genomics 47, 681-693. (10.1016/j.jgg.2020.10.005) PubMed DOI
Pessia E, Makino T, Bailly-Bechet M, McLysaght A, Marais GAB. 2012. Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proc. Natl Acad. Sci. USA 109, 5346-5351. (10.1073/pnas.1116763109) PubMed DOI PMC
Pessia E, Engelstädter J, Marais GAB. 2014. The evolution of X chromosome inactivation in mammals: the demise of Ohno's hypothesis? Cell Mol. Life Sci. 71, 1383-1394. (10.1007/s00018-013-1499-6) PubMed DOI PMC
Birchler JA. 2012. Claims and counterclaims of X-chromosome compensation. Nat. Struct. Mol. Biol. 19, 3-5. (10.1038/nsmb.2218) PubMed DOI
Julien P, Brawand D, Soumillon M, Necsulea A, Liechti A, Schütz F, Daish T, Grützner F, Kaessmann H. 2012. Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol. 10, e1001328. (10.1371/journal.pbio.1001328) PubMed DOI PMC
Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434, 400-404. (10.1038/nature03479) PubMed DOI
Muyle A, Bachtrog D, Marais GAB, Turner JMA. 2021. Epigenetics drive the evolution of sex chromosomes in animals and plants. Phil. Trans. R. Soc. B 376, 20200124. (10.1098/rstb.2020.0124) PubMed DOI PMC
Lenormand T, Fyon F, Sun E, Roze D. 2020. Sex chromosome degeneration by regulatory evolution. Curr. Biol. 30, 3001-3006. (10.1016/j.cub.2020.05.052) PubMed DOI
Deakin JE, Deakin JE. 2013. Marsupial X chromosome inactivation: past, present and future. Aust. J. Zool. 61, 13-23. (10.1071/ZO12113) DOI
Csankovszki G. 2009. Condensin function in dosage compensation. Epigenetics 4, 212-215. (10.4161/epi.8957) PubMed DOI
Ercan S, Lieb JD. 2009. C. elegans dosage compensation: a window into mechanisms of domain-scale gene regulation. Chromosome Res. 17, 215-227. (10.1007/s10577-008-9011-0) PubMed DOI
Meyer BJ. 2010. Targeting X chromosomes for repression. Curr. Opin. Genet. Dev. 20, 179-189. (10.1016/j.gde.2010.03.008) PubMed DOI PMC
Albritton SE, Kranz AL, Rao P, Kramer M, Dieterich C, Ercan S. 2014. Sex-biased gene expression and evolution of the x chromosome in nematodes. Genetics 197, 865-883. (10.1534/genetics.114.163311) PubMed DOI PMC
Malone JH, et al. 2012. Mediation of Drosophila autosomal dosage effects and compensation by network interactions. Genome Biol. 13, r28. (10.1186/gb-2012-13-4-r28) PubMed DOI PMC
Hose J, Yong CM, Sardi M, Wang Z, Newton MA, Gasch AP. 2015. Dosage compensation can buffer copy-number variation in wild yeast. Elife 4, e05462. (10.7554/eLife.05462) PubMed DOI PMC
Gu L, Walters JR. 2017. Evolution of sex chromosome dosage compensation in animals: a beautiful theory, undermined by facts and bedeviled by details. Genome Biol. Evol. 9, 2461-2476. (10.1093/gbe/evx154) PubMed DOI PMC
Chandler CH. 2017. When and why does sex chromosome dosage compensation evolve? Ann. N. Y. Acad. Sci. 1389, 37-51. (10.1111/nyas.13307) PubMed DOI
Mank JE. 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends Genet. 29, 677-683. (10.1016/j.tig.2013.07.005) PubMed DOI
Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D. 2013. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 11, e1001643. (10.1371/journal.pbio.1001643) PubMed DOI PMC
Ellegren H, Hultin-Rosenberg L, Brunström B, Dencker L, Kultima K, Scholz B. 2007. Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol. 5, 40. (10.1186/1741-7007-5-40) PubMed DOI PMC
Catalán A, Merondun J, Knief U, Wolf JBW. 2021. Epigenetic mechanisms of partial dosage compensation in an avian, female heterogametic system. bioRxiv, 2021.08.17.456618. (10.1101/2021.08.17.456618) DOI
Ellison CE, Bachtrog D. 2013. Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342, 846-850. (10.1126/science.1239552) PubMed DOI PMC
Ellison C, Bachtrog D. 2019. Recurrent gene co-amplification on Drosophila X and Y chromosomes. PLoS Genet. 15, e1008251. (10.1371/journal.pgen.1008251) PubMed DOI PMC
Veyrunes F, et al. 2008. Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18, 965-973. (10.1101/gr.7101908) PubMed DOI PMC
Renner SS. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101, 1588-1596. (10.3732/ajb.1400196) PubMed DOI
Charlesworth D. 2021. When and how do sex-linked regions become sex chromosomes? Evolution 75, 569-581. (10.1111/evo.14196) PubMed DOI
Renner SS, Müller NA. 2021. Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration. Nat. Plants 7, 392-402. (10.1038/s41477-021-00884-3) PubMed DOI
Muyle A, Käfer J, Zemp N, Mousset S, Picard F, Marais GA. 2016. SEX-DETector: a probabilistic approach to study sex chromosomes in non-model organisms. Genome Biol. Evol. 8, 2530-2543. (10.1093/gbe/evw172) PubMed DOI PMC
Muyle A, Shearn R, Marais GA. 2017. The evolution of sex chromosomes and dosage compensation in plants. Genome Biol. Evol. 9, 627-645. (10.1093/gbe/evw282) PubMed DOI PMC
Palmer DH, Rogers TF, Dean R, Wright AE. 2019. How to identify sex chromosomes and their turnover. Mol. Ecol. 28, 4709-4724. (10.1111/mec.15245) PubMed DOI PMC
Michalovova M, Kubat Z, Hobza R, Vyskot B, Kejnovsky E. 2015. Fully automated pipeline for detection of sex linked genes using RNA-Seq data. BMC Bioinf. 16, 78. (10.1186/s12859-015-0509-0) PubMed DOI PMC
Vicoso B, Bachtrog D. 2009. Progress and prospects toward our understanding of the evolution of dosage compensation. Chromosome Res. 17, 585-602. (10.1007/s10577-009-9053-y) PubMed DOI PMC
Vyskot B. 1999. The role of DNA methylation in plant reproductive development. In Sex determination in plants (eds CC Ainsworth), pp. 101-122. BIOS Scientific Publishers Ltd, Oxford.
Bernasconi G, et al. 2009. Silene as a model system in ecology and evolution. Heredity (Edinb) 103, 5-14. (10.1038/hdy.2009.34) PubMed DOI
Westergaard M. 1946. Structural changes of the Y chromosome in the offspring of polyploid Melandrium. Hereditas 32, 60-64. (10.1111/j.1601-5223.1946.tb02771.x) PubMed DOI
Westergaard M. 1946. Aberrant Y chromosomes and sex expression in Melandrium album. Hereditas 32, 419-443. (10.1111/j.1601-5223.1946.tb02784.x) PubMed DOI
Warmke HE. 1946. An analysis of male development in Melandrium by means of Y chromosome deficiencies. Genetics 31, 234. PubMed
Westergaard M. 1958. The mechanism of sex determination in dioecious flowering plants. Adv. Genet. 9, 217-281. (10.1016/s0065-2660(08)60163-7) PubMed DOI
Krasovec M, Chester M, Ridout K, Filatov DA. 2018. The mutation rate and the age of the sex chromosomes in Silene latifolia. Curr. Biol. 28, 1832-1838. (10.1016/j.cub.2018.04.069) PubMed DOI
Bačovský V, Čegan R, Šimoníková D, Hřibová E, Hobza R. 2020. The formation of sex chromosomes in Silene latifolia and S. dioica was accompanied by multiple chromosomal rearrangements. Front. Plant Sci. 11, 205. (10.3389/fpls.2020.00205) PubMed DOI PMC
Vyskot B, Araya A, Veuskens J, Negrutiu I, Mouras A. 1993. DNA methylation of sex chromosomes in a dioecious plant, Melandrium album. Mol. Gen. Genet. 239, 219-224. (10.1007/BF00281621) PubMed DOI
Siroky J, Castiglione MR, Vyskot B. 1998. DNA methylation patterns of Melandrium album chromosomes. Chromosome Res. 6, 441-446. (10.1023/A:1009244210622) PubMed DOI
Široký J, Janoušek B, Mouras A, Vyskot B. 1994. Replication patterns of sex chromosomes in Melandrium album female cells. Hereditas 120, 175-181. (10.1111/j.1601-5223.1994.00175.x) DOI
Bačovský V, Houben A, Kumke K, Hobza R. 2019. The distribution of epigenetic histone marks differs between the X and Y chromosomes in Silene latifolia. Planta 250, 487-494. (10.1007/s00425-019-03182-7) PubMed DOI
Muyle A, Zemp N, Deschamps C, Mousset S, Widmer A, Marais GAB. 2012. Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol. 10, e1001308. (10.1371/journal.pbio.1001308) PubMed DOI PMC
Bergero R, Qiu S, Charlesworth D. 2015. Gene loss from a plant sex chromosome system. Curr. Biol. 25, 1234-1240. (10.1016/j.cub.2015.03.015) PubMed DOI
Papadopulos AST, Chester M, Ridout K, Filatov DA. 2015. Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proc. Natl Acad. Sci. USA 112, 13 021-13 026. (10.1073/pnas.1508454112) PubMed DOI PMC
Muyle A, et al. 2018. Genomic imprinting mediates dosage compensation in a young plant XY system. Nat. Plants 4, 677-680. (10.1038/s41477-018-0221-y) PubMed DOI
Choudhuri HC. 1969. Late DNA replication pattern in sex chromosomes of Melandrium. Can. J. Genet. Cytol. 11, 192-198. (10.1139/g69-023) PubMed DOI
Kampmeijer P. 1972. Fluorescence pattern of the sex-chromosomes of Melandrium dioicum, stained with quinacrine-mustard. Genetica 43, 201-206. (10.1007/BF00123626) DOI
Siroky J, Hodurkova J, Negrutiu I, Vyskot B. 1999. Functional and structural chromosome analyses in autotetraploid Silene latifolia. Ann. Bot. 84, 633-638. (10.1006/anbo.1999.0958) DOI
Vyskot B, Siroky J, Hladilova R, Belyaev ND, Turner BM. 1999. Euchromatic domains in plant chromosomes as revealed by H4 histone acetylation and early DNA replication. Genome 42, 343-350. (10.1139/g98-133) PubMed DOI
Jamieson RV, Tam PP, Gardiner-Garden M. 1996. X-chromosome activity: impact of imprinting and chromatin structure. Int. J. Dev. Biol. 40, 1065-1080. PubMed
Janousek B, Siroký J, Vyskot B. 1996. Epigenetic control of sexual phenotype in a dioecious plant, Melandrium album. Mol. Gen. Genet. 250, 483-490. (10.1007/BF02174037) PubMed DOI
Bačovský V, Čegan R, Tihlaříková E, Neděla V, Hudzieczek V, Smrža L, Beneš V, Hobza R. 2021. Identification of developmentally important genes in Silene latifolia through chemical genetics and transcriptome profiling. bioRxiv, 2021.01.25.428076. (10.1101/2021.01.25.428076) PubMed DOI
Chibalina MV, Filatov DA. 2011. Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr. Biol. 21, 1475-1479. (10.1016/j.cub.2011.07.045) PubMed DOI
Bergero R, Charlesworth D. 2011. Preservation of the Y transcriptome in a 10-million-year-old plant sex chromosome system. Curr. Biol. 21, 1470-1474. (10.1016/j.cub.2011.07.032) PubMed DOI
Kazama Y, Nishihara K, Bergero R, Fujiwara MT, Abe T, Charlesworth D, Kawano S. 2012. SlWUS1; an X-linked gene having no homologous Y-linked copy in Silene latifolia. G3 (Bethesda) 2, 1269-1278. (10.1534/g3.112.003749) PubMed DOI PMC
Toups M, Veltsos P, Pannell JR. 2015. Plant sex chromosomes: lost genes with little compensation. Curr. Biol. 25, R427-R430. (10.1016/j.cub.2015.03.054) PubMed DOI
Blavet N, et al. 2015. Identifying new sex-linked genes through BAC sequencing in the dioecious plant Silene latifolia. BMC Genomics 16, 546. (10.1186/s12864-015-1698-7) PubMed DOI PMC
Crowson D, Barrett SCH, Wright SI. 2017. Purifying and positive selection influence patterns of gene loss and gene expression in the evolution of a plant sex chromosome system. Mol. Biol. Evol. 34, 1140-1154. (10.1093/molbev/msx064) PubMed DOI
Charlesworth D. 2019. Young sex chromosomes in plants and animals. New Phytol. 224, 1095-1107. (10.1111/nph.16002) PubMed DOI
Krasovec M, Kazama Y, Ishii K, Abe T, Filatov DA. 2019. Immediate dosage compensation is triggered by the deletion of Y-linked genes in Silene latifolia. Curr. Biol. 29, 2214-2221. (10.1016/j.cub.2019.05.060) PubMed DOI PMC
Lorenzo JL R, Hubinský M, Vyskot B, Hobza R. 2020. Histone post-translational modifications in Silene latifolia X and Y chromosomes suggest a mammal-like dosage compensation system. Plant Sci. 299, 110528. (10.1016/j.plantsci.2020.110528) PubMed DOI
Lyon MF. 1998. X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80, 133-137. (10.1159/000014969) PubMed DOI
Cotton AM, Chen CY, Lam LL, Wasserman WW, Kobor MS, Brown CJ. 2014. Spread of X-chromosome inactivation into autosomal sequences: role for DNA elements, chromatin features and chromosomal domains. Hum. Mol. Genet. 23, 1211-1223. (10.1093/hmg/ddt513) PubMed DOI PMC
Tannan NB, Brahmachary M, Garg P, Borel C, Alnefaie R, Watson CT, Thomas NS, Sharp AJ. 2014. DNA methylation profiling in X;autosome translocations supports a role for L1 repeats in the spread of X chromosome inactivation. Hum. Mol. Genet. 23, 1224-1236. (10.1093/hmg/ddt553) PubMed DOI PMC
Popova BC, Tada T, Takagi N, Brockdorff N, Nesterova TB. 2006. Attenuated spread of X-inactivation in an X;autosome translocation. Proc. Natl Acad Sci. USA 103, 7706-7711. (10.1073/pnas.0602021103) PubMed DOI PMC
Kubat Z, Zluvova J, Vogel I, Kovacova V, Cermak T, Cegan R, Hobza R, Vyskot B, Kejnovsky E. 2014. Possible mechanisms responsible for absence of a retrotransposon family on a plant Y chromosome. New Phytol. 202, 662-678. (10.1111/nph.12669) PubMed DOI
Filatov DA, Howell EC, Groutides C, Armstrong SJ. 2009. Recent spread of a retrotransposon in the Silene latifolia genome, apart from the Y chromosome. Genetics 181, 811-817. (10.1534/genetics.108.099267) PubMed DOI PMC
Kralova T, Cegan R, Kubat Z, Vrana J, Vyskot B, Vogel I, Kejnovsky E, Hobza R. 2014. Identification of a novel retrotransposon with sex chromosome-specific distribution in Silene latifolia. Cytogenet. Genome Res. 143, 87-95. (10.1159/000362142) PubMed DOI
Cermak T, Kubat Z, Hobza R, Koblizkova A, Widmer A, Macas J, Vyskot B, Kejnovsky E. 2008. Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Res. 16, 961-976. (10.1007/s10577-008-1254-2) PubMed DOI
Prentout D, Stajner N, Cerenak A, Tricou T, Brochier-Armanet C, Jakse J, Käfer J, Marais GAB. 2021. Plant genera Cannabis and Humulus share the same pair of well-differentiated sex chromosomes. New Phytol. 231, 1599-1611. (10.1111/nph.17456) PubMed DOI
Prentout D, Razumova O, Rhoné B, Badouin H, Henri H, Feng C, Käfer J, Karlov G, Marais GAB. 2020. An efficient RNA-seq-based segregation analysis identifies the sex chromosomes of Cannabis sativa. Genome Res. 30, 164-172. (10.1101/gr.251207.119) PubMed DOI PMC
Divashuk MG, Alexandrov OS, Razumova OV, Kirov IV, Karlov GI. 2014. Molecular cytogenetic characterization of the dioecious Cannabis sativa with an XY chromosome sex determination system. PLoS ONE 9, e85118. (10.1371/journal.pone.0085118) PubMed DOI PMC
Divashuk MG, Alexandrov OS, Kroupin PY, Karlov GI. 2011. Molecular cytogenetic mapping of Humulus lupulus sex chromosomes. Cytogenet. Genome Res. 134, 213-219. (10.1159/000328831) PubMed DOI
Shephard HL, Parker JS, Darby P, Ainsworth CC. 2000. Sexual development and sex chromosomes in hop. New Phytol. 148, 397-411. (10.1046/j.1469-8137.2000.00771.x) PubMed DOI
Holstein N, Renner SS. 2011. A dated phylogeny and collection records reveal repeated biome shifts in the African genus Coccinia (Cucurbitaceae). BMC Evol. Biol. 11, 28. (10.1186/1471-2148-11-28) PubMed DOI PMC
Fruchard C, et al. 2020. Evidence for dosage compensation in Coccinia grandis, a plant with a highly heteromorphic XY system. Genes (Basel) 11, 787. (10.3390/genes11070787) PubMed DOI PMC
Hough J, Hollister JD, Wang W, Barrett SCH, Wright SI. 2014. Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus. Proc. Natl Acad. Sci. USA 111, 7713-7718. (10.1073/pnas.1319227111) PubMed DOI PMC
Wang J, et al. 2012. Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc. Natl Acad. Sci. USA 109, 13 710-13 715. (10.1073/pnas.1207833109) PubMed DOI PMC
Liu J, Han J, Sharma A, Wai CM, Ming R, Yu Q. 2021. Transcriptional regulation of dosage compensation in Carica papaya. Sci. Rep. 11, 5854. (10.1038/s41598-021-85480-3) PubMed DOI PMC
Chae T, Harkess A, Moore RC. 2021. Sex-linked gene expression and the emergence of hermaphrodites in Carica papaya. Am. J. Bot. 108, 1029-1041. (10.1002/ajb2.1689) PubMed DOI
Balounova V, et al. 2019. Evolution of sex determination and heterogamety changes in section Otites of the genus Silene. Sci. Rep. 9, 1045. (10.1038/s41598-018-37412-x) PubMed DOI PMC
Martin H, Carpentier F, Gallina S, Godé C, Schmitt E, Muyle A, Marais GA, Touzet P. 2019. Evolution of young sex chromosomes in two dioecious sister plant species with distinct sex determination systems. Genome Biol. Evol. 11, 350-361. (10.1093/gbe/evz001) PubMed DOI PMC
Veltsos P, et al. 2019. Early sex-chromosome evolution in the diploid dioecious plant Mercurialis annua. Genetics 212, 815-835. (10.1534/genetics.119.302045) PubMed DOI PMC
Muller H. 1950. Evidence of the precision of genetic adaptation. Harvey Lect. 43, 165-229.
Charlesworth B. 1996. The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6, 149-162. (10.1016/S0960-9822(02)00448-7) PubMed DOI
Engelstädter J, Haig D. 2008. Sexual antagonism and the evolution of X chromosome inactivation. Evolution 62, 2097-2104. (10.1111/j.1558-5646.2008.00431.x) PubMed DOI
Bachtrog D. 2008. The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179, 1513-1525. (10.1534/genetics.107.084012) PubMed DOI PMC
Engelstädter J. 2008. Muller's ratchet and the degeneration of Y chromosomes: a simulation study. Genetics 180, 957-967. (10.1534/genetics.108.092379) PubMed DOI PMC
Schultheiß R, Viitaniemi HM, Leder EH. 2015. Spatial dynamics of evolving dosage compensation in a young sex chromosome system. Genome Biol. Evol. 7, 581-590. (10.1093/gbe/evv013) PubMed DOI PMC
Metzger DCH, Schulte PM. 2018. The DNA methylation landscape of stickleback reveals patterns of sex chromosome evolution and effects of environmental salinity. Genome Biol. Evol. 10, 775-785. (10.1093/gbe/evy034) PubMed DOI PMC
Darolti I, et al. 2019. Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers. Proc. Natl Acad. Sci. USA 116, 19 031-19 036. (10.1073/pnas.1905298116) PubMed DOI PMC
Rice W. 1987. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution 41, 911-914. (10.2307/2408899) PubMed DOI
Haig D. 2006. Self-imposed silence: parental antagonism and the evolution of X-chromosome inactivation. Evolution 60, 440-447. (10.1111/j.0014-3820.2006.tb01125.x) PubMed DOI
Haig D. 2006. Intragenomic politics. Cytogenet. Genome Res. 113, 68-74. (10.1159/000090816) PubMed DOI
Cailleau A, Grimanelli D, Blanchet E, Cheptou PO, Lenormand T. 2018. Dividing a maternal pie among half-sibs: genetic conflicts and the control of resource allocation to seeds in maize. Am. Nat. 192, 577-592. (10.1086/699653) PubMed DOI
Wilkins JF, Haig D. 2003. What good is genomic imprinting: the function of parent-specific gene expression. Nat. Rev. Genet. 4, 359-368. (10.1038/nrg1062) PubMed DOI
Patten MM, Ross L, Curley JP, Queller DC, Bonduriansky R, Wolf JB. 2014. The evolution of genomic imprinting: theories, predictions and empirical tests. Heredity (Edinb.) 113, 119-128. (10.1038/hdy.2014.29) PubMed DOI PMC
Baroux C, Spillane C, Grossniklaus U. 2002. Genomic imprinting during seed development. Adv. Genet. 46, 165-214. (10.1016/s0065-2660(02)46007-5) PubMed DOI
Graves JAM. 2016. Evolution of vertebrate sex chromosomes and dosage compensation. Nat. Rev. Genet. 17, 33-46. (10.1038/nrg.2015.2) PubMed DOI
Mullon C, Wright AE, Reuter M, Pomiankowski A, Mank JE. 2015. Evolution of dosage compensation under sexual selection differs between X and Z chromosomes. Nat. Commun. 6, 7720. (10.1038/ncomms8720) PubMed DOI PMC
Sexy ways: approaches to studying plant sex chromosomes
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