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Deciphering evolutionary strata on plant sex chromosomes and fungal mating-type chromosomes through compositional segmentation

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Abstract

Sex chromosomes have evolved from a pair of homologous autosomes which differentiated into sex determination systems, such as XY or ZW system, as a consequence of successive recombination suppression between the gametologous chromosomes. Identifying the regions of recombination suppression, namely, the “evolutionary strata”, is central to understanding the history and dynamics of sex chromosome evolution. Evolution of sex chromosomes as a consequence of serial recombination suppressions is well-studied for mammals and birds, but not for plants, although 48 dioecious plants have already been reported. Only two plants Silene latifolia and papaya have been studied until now for the presence of evolutionary strata on their X chromosomes, made possible by the sequencing of sex-linked genes on both the X and Y chromosomes, which is a requirement of all current methods that determine stratum structure based on the comparison of gametologous sex chromosomes. To circumvent this limitation and detect strata even if only the sequence of sex chromosome in the homogametic sex (i.e. X or Z chromosome) is available, we have developed an integrated segmentation and clustering method. In application to gene sequences on the papaya X chromosome and protein-coding sequences on the S. latifolia X chromosome, our method could decipher all known evolutionary strata, as reported by previous studies. Our method, after validating on known strata on the papaya and S. latifolia X chromosome, was applied to the chromosome 19 of Populus trichocarpa, an incipient sex chromosome, deciphering two, yet unknown, evolutionary strata. In addition, we applied this approach to the recently sequenced sex chromosome V of the brown alga Ectocarpus sp. that has a haploid sex determination system (UV system) recovering the sex determining and pseudoautosomal regions, and then to the mating-type chromosomes of an anther-smut fungus Microbotryum lychnidis-dioicae predicting five strata in the non-recombining region of both the chromosomes.

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References

  • Ahmed S, Cock JM, Pessia E, Luthringer R, Cormier A, Robuchon M, Sterck L, Peter AF, Dittami SM, Corre E et al (2014) A haploid system of sex determination in the brown alga Ectocarpus sp. Curr Biol 24(17):1945–1957

    Article  CAS  PubMed  Google Scholar 

  • Arvey AJ, Azad RK, Raval A, Lawrence JG (2009) Detection of genomic islands via segmental genome heterogeneity. Nucleic Acids Res 37:5255–5266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azad RK, Li J (2013) Interpreting genomic data via entropic dissection. Nucleic Acids Res 41:e23

    Article  CAS  PubMed  Google Scholar 

  • Azad RK, Bernaola-Galvan P, Ramaswamy R, Rao JS (2002) Segmentation of genomic DNA through entropic divergence: power laws and scaling. Phys Rev E Stat Nonlin Soft Matter Phys 65: Epub 051909

  • Bachtrog D (2008) The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179:1513–1525

    Article  PubMed  PubMed Central  Google Scholar 

  • Bachtrog D (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badouin H, Hood ME, Gouzy J, Aguileta G, Siguenza S, Perlin MH, Cuomo CA, Fairhead C, Branca A, Giraud T (2015) Chaos of rearrangements in the mating-type chromosomes of the anther-smut fungus Microbotryum Lychnidis-dioicae. Genetics 200(4):1275–1284

    Article  PubMed  PubMed Central  Google Scholar 

  • Bergero R, Charlesworth D (2011) Preservation of the Y transcriptome in a 10 MY old plant sex chromosome system. Curr Biol 21:1470–1474

    Article  CAS  PubMed  Google Scholar 

  • Bergero R, Forrest A, Kamau E, Charlesworth D (2007) Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics 175:1945–1954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergero R, Qiu S, Forrest A, Borthwick H, Charlesworth D (2013) Expansion of the pseudo-autosomal region and ongoing recombination suppression in the Silene latifolia sex chromosomes. Genetics 194:673–686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernaola-Galvan P, Roman-Roldan R, Oliver JL (1996) Compositional segmentation and long-range fractal correlations in DNA sequences. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 53:5181–5189

    CAS  PubMed  Google Scholar 

  • Brookfield JFY (1991) Models of repression of transposition in P-M hybrid dysgenesis by P cytotype and by zygotically encoded repressor proteins. Genetics 128:471–486

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth B (1978) Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci USA 75:5618–5622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Phil Trans R Soc Lond B Biol Sci 355:1563–1572

    Article  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95(2):118–128

    Article  CAS  PubMed  Google Scholar 

  • Dolgin ES, Charlesworth B (2008) The effects of recombination rate on the distribution and abundance of transposable elements. Genetics 178(4):2169–2177

    Article  PubMed  PubMed Central  Google Scholar 

  • Filatov DA (2005) Evolutionary history of Silene latifolia sex chromosomes revealed by genetic map** of four genes. Genetics 170:975–979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finnegan DJ (1992) Transposable elements. The Genome of Drosophila melanogaster, pp 1096–1107

  • Fontanillas E, Hood M, Badouin H, Petit E, Barbe V, Gouzy J, deVienne DM, Aguileta G, Poulain J, Wincker P, Chen Z et al (2015) Degeneration of the non-recombining regions in the mating type chromosomes of the anther smut fungi. Mol Biol Evol 32:928–943

    Article  CAS  PubMed  Google Scholar 

  • Gaudet M, Jorge V, Paolucci I, Beritognolo I, Mugnozza G, Sabatti M (2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes 4:25–36

    Article  Google Scholar 

  • Geraldes A, Hefer CA, Capron A, Kolosova N, MartinezNuñez F, Soolanayakanahally RY, Stanton B, Guy RD, Mansfield S, Douglas CJ, Cronk QCB (2015) Recent Y chromosome divergence despite ancient origin of dioecy in poplars (Populus). Mol Ecol 24(13):3243–3256

    Article  CAS  PubMed  Google Scholar 

  • Grosse I, Bernaola-Galvan P, Carpena P, Roman-Roldan R, Oliver J, Stanley HE (2002) Analysis of symbolic sequences using the Jensen-Shannon divergence. Phys Rev E Stat Nonlin Soft Matter Phys 65:041905

    Article  PubMed  Google Scholar 

  • Hobza R, Kejnovsky E, Vyskot B, Widmer A (2007) The role of chromosomal rearrangements in the evolution of Silene latifolia sex chromosomes. Mol Genet Genomics 278:633–638

    Article  CAS  PubMed  Google Scholar 

  • Hood ME, Antonovics J, Koskella B (2004) Shared forces of sex chromosome evolution in haploids-mating and diploids-mating organisms: Microbotryum violaceum and other model organisms. Genetics 168:141–146

    Article  PubMed  PubMed Central  Google Scholar 

  • Hood ME, Petit E, Giraud T (2013) Extensive divergence between mating-type chromosomes of the anther-smut fungus. Genetics 193:309–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou J, Ning Y, Defang Z, Yingnan C, Lecheng F, **aogang D, Tongming Y (2015) Different autosomes evolved into sex chromosomes in the sister genera of Salix and Populus. Sci Rep 5:9076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jordan C, Charlesworth D (2012) The potential for sexually antagonistic polymorphism in different genome regions. Evolution 66:505–516

    Article  PubMed  Google Scholar 

  • Kirkpatrick M, Barton N (2006) Chromosome inversions, local adaptation and speciation. Genetics 173:419–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964–967

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre C, Braga MD, Gautier C, Sagot MF, Tannier E, Marais GA (2009a) Footprints of inversions at present and past pseudoautosomal boundaries in human sex chromosomes. Genome Biol Evol 1:56–66

    Article  PubMed  PubMed Central  Google Scholar 

  • Lemaitre JF, Ramm SA, Barton RA, Stockley P (2009b) Sperm competition and brain size evolution in mammals. J Evol Biol 22:2215–2221

    Article  PubMed  Google Scholar 

  • Li Wentian (2001) New stop** criteria for segmenting DNA sequences. Phys Rev Lett 86:5815–5818

    Article  CAS  PubMed  Google Scholar 

  • Lin J (1991) Divergence measures based on the Shannon entropy. IEEE Trans Inform Theory 37:145–151

    Article  Google Scholar 

  • Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, Pearl HM, Kim MS, Charlton JW, Ming R et al (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427:348–352

    Article  CAS  PubMed  Google Scholar 

  • Ming R, Moore PH (2007) Genomics of sex chromosomes. Curr Opin Plant Biol 10:123–130

    Article  CAS  PubMed  Google Scholar 

  • Ming R, Bendahmane A, Renner SS (2011) Sex chromosome in land plants. Annu Rev Plant Biol 62:485–514

    Article  CAS  PubMed  Google Scholar 

  • Montgomery EA, Charlesworth B, Langley CH (1987) A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res 49:31–41

    Article  CAS  PubMed  Google Scholar 

  • Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9

    Article  Google Scholar 

  • Nam K, Ellegren H (2008) The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 180:1131–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M (1970) Accumulation of nonfunctional genes on sheltered chromosomes. Am Nat 104:311–322

    Article  Google Scholar 

  • Pandey RS, Wilson MA, Azad RK (2013) Detecting evolutionary strata on the human X chromosome in the absence of gametologous Y-linked sequences. Genome Biol Evol 5:1863–1871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rice WR (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735–742

    Article  Google Scholar 

  • Rice WR (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

    Article  Google Scholar 

  • Rice WR (1996) Evolution of the Y sex chromosome in animals. Biosciences 46:331–343

    Article  Google Scholar 

  • Ross MT, Grafham DV, Coffey AJ, Scherer S, Mclay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP et al (2005) The DNA sequence of the human X chromosome. Nature 434:325–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandstedt SA, Tucker PK (2004) Evolutionary strata on the mouse X chromosome correspond to strata on the human X chromosome. Genome Res 14:267–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Rep** S, Pyntikova T, Ali J, Bieri T et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837

    Article  CAS  PubMed  Google Scholar 

  • Smit AFA, Hubley R, Green P (2013–2015) RepeatMakser Open-4.0. http://www.repeatmasker.org

  • Sterck L, Billiau K, Abeel T, Rouze P, Van de Peer Y (2012) ORCAE: online resource for community annotation of eukaryotes. Nat Methods 9:1041

    Article  CAS  PubMed  Google Scholar 

  • Thakur V, Azad RK, Ramaswamy R (2007) Markov models of genome segmentation. Phys Rev E Stat Nonlin Soft Matter Phys 75:011915

    Article  PubMed  Google Scholar 

  • Tuskan GA, DiFazio S, Faivre-Rampant P, Gaudet M, Harfouche A, Jorge V, Labbe JL, Ranjan P, Sabatti M, Salavov G et al (2012) The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis. True Genet Genomics 8:559–571

    Article  Google Scholar 

  • Veyrunes F, Waters PD, Miethke P, Rens W, McMillan D, Alsop AE, Grutzner F, Deakin JE, Whittington CM, Schatzkamer K et al (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18:965–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Votintseva AA, Filatov DA (2009) Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics 182:1391–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Na JK, Yu Q, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, Zhang W et al (2012) Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci USA 109:13710–13715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittle CA, Votintseva A, Ridout K, Filatov DA (2015) Recent and massive expansion of the mating-type specific region in the smut fungus Microbotryum. Genetics 199:809–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson MA, Makova KD (2009) Evolution and survival on eutherian sex chromosomes. PLoS Genet 5:e1000568

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson MA, Makova KD (2013) Gene survival and death on the human Y chromosome. Mol Biol Evol 30:781–787

    Article  Google Scholar 

  • Yin T, Difazio SP, Gunter LE, Zhang X, Sewell MM, Woolbright SA, Allan GJ, Kelleher CT, Douglas CJ, Wang M et al (2008) Genome structure and emerging evidence of an incipient sex chromosome in Populus. Genome Res 18:422–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Navajas-Pérez R, Tong E, Robertson J, Moore PH, Paterson AH, Ray Ming R (2008) Recent origin of dioecious and gynodioecious Y chromosomes in papaya. Trop Plant Biol 1:49–57

    Article  Google Scholar 

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Acknowledgments

This work was supported by a faculty start-up fund and JFSRF award from the University of North Texas to RKA and a Beth Baird graduate student scholarship to RSP.

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Authors and Affiliations

  1. Department of Biological Sciences, University of North Texas, Denton, TX, USA

    Ravi S. Pandey & Rajeev K. Azad

  2. Department of Mathematics, University of North Texas, Denton, TX, USA

    Rajeev K. Azad

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  1. Ravi S. Pandey
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  2. Rajeev K. Azad
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Correspondence to Rajeev K. Azad.

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Pandey, R.S., Azad, R.K. Deciphering evolutionary strata on plant sex chromosomes and fungal mating-type chromosomes through compositional segmentation. Plant Mol Biol 90, 359–373 (2016). https://doi.org/10.1007/s11103-015-0422-y

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