Chromosome fusions shape an ancient UV sex chromosome system

Sex chromosomes occur in diverse organisms, but their structural complexity has often prevented evolutionary analyses. Here we use two chromosome-scale reference genomes of the moss Ceratodon purpureus to trace the evolution of the sex chromosomes in bryophytes. Comparative analyses show the moss genome comprises seven remarkably stable ancestral chromosomal elements. An exception is the sex chromosomes, which share thousands of broadly-expressed genes but lack any synteny. We show the sex chromosomes evolved over 300 million years ago and expanded via at least two distinct chromosomal fusions. These results link suppressed recombination between the sex chromosomes with rapid structural change and the evolution of distinct transposable element compositions, and suggest haploid gene expression promotes the evolution of independent female and male gene-regulatory networks. One Sentence Summary Moss sex chromosomes retain thousands of broadly-expressed genes despite millions of years of suppressed recombination.

[1]  J. Bull.  Sex Chromosomes in Haploid Dioecy: A Unique Contrast to Muller's Theory for Diploid Dioecy , 1978, The American Naturalist.

[2]  V. Jagannathan,et al.  Blackboard Architectures and Applications , 1989 .

[3]  R. Fritsch.  Index to bryophyte chromosome counts , 1991 .

[4]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[5]  P Green,et al.  Base-calling of automated sequencer traces using phred. II. Error probabilities. , 1998, Genome research.

[6]  P. Green,et al.  Base-calling of automated sequencer traces using phred. I. Accuracy assessment. , 1998, Genome research.

[7]  P. Green,et al.  Consed: a graphical tool for sequence finishing. , 1998, Genome research.

[8]  Robert D. Finn,et al.  Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins , 1999, Nucleic Acids Res..

[9]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[10]  D. Page,et al.  Four evolutionary strata on the human X chromosome. , 1999, Science.

[11]  B. Charlesworth,et al.  The degeneration of Y chromosomes. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  Susumu Goto,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[13]  V. Solovyev,et al.  Ab initio gene finding in Drosophila genomic DNA. , 2000, Genome research.

[14]  G. Roeder,et al.  The Mnd1 Protein Forms a Complex with Hop2 To Promote Homologous Chromosome Pairing and Meiotic Double-Strand Break Repair , 2002, Molecular and Cellular Biology.

[15]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[16]  Anton J. Enright,et al.  An efficient algorithm for large-scale detection of protein families. , 2002, Nucleic acids research.

[17]  R. Wing,et al.  An improved method for plant BAC library construction. , 2003, Methods in molecular biology.

[18]  T. Graves,et al.  The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes , 2003, Nature.

[19]  Stephen M. Mount,et al.  Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. , 2003, Nucleic acids research.

[20]  Ewan Birney,et al.  Automated generation of heuristics for biological sequence comparison , 2005, BMC Bioinformatics.

[21]  S. McDaniel,et al.  Selective sweeps and intercontinental migration in the cosmopolitan moss Ceratodon purpureus (Hedw.) Brid. , 2005, Molecular ecology.

[22]  GENETIC CORRELATIONS DO NOT CONSTRAIN THE EVOLUTION OF SEXUAL DIMORPHISM IN THE MOSS CERATODON PURPUREUS , 2005, Evolution; international journal of organic evolution.

[23]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[24]  Casey M. Bergman,et al.  Combined Evidence Annotation of Transposable Elements in Genome Sequences , 2005, PLoS Comput. Biol..

[25]  Gábor Csárdi,et al.  The igraph software package for complex network research , 2006 .

[26]  D. Haig,et al.  Sexual conflict and the alternation of haploid and diploid generations , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  Adam Godzik,et al.  Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences , 2006, Bioinform..

[28]  Jun Li,et al.  KaKs_Calculator: Calculating Ka and Ks Through Model Selection and Model Averaging , 2007, Genom. Proteom. Bioinform..

[29]  Peer Bork,et al.  PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments , 2006, Nucleic Acids Res..

[30]  Thomas Rattei,et al.  Gepard: a rapid and sensitive tool for creating dotplots on genome scale , 2007, Bioinform..

[31]  M. Kirkpatrick,et al.  Turnover of sex chromosomes induced by sexual conflict , 2007, Nature.

[32]  Ralf Reski,et al.  An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens , 2007, BMC Evolutionary Biology.

[33]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[34]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[35]  S. M. Eppley,et al.  Moving to mate: the evolution of separate and combined sexes in multicellular organisms , 2008, Journal of evolutionary biology.

[36]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[37]  R. Quatrano,et al.  Culturing the moss Physcomitrella patens. , 2009, Cold Spring Harbor protocols.

[38]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[39]  Gao Yu,et al.  Design of integrated system for heterogeneous network query terminal: Design of integrated system for heterogeneous network query terminal , 2009 .

[40]  J. Graves,et al.  Physical mapping of the elephant X chromosome: conservation of gene order over 105 million years , 2009, Chromosome Research.

[41]  D. Charlesworth,et al.  The evolution of restricted recombination in sex chromosomes. , 2009, Trends in ecology & evolution.

[42]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[43]  Yibo Wu,et al.  GOSemSim: an R package for measuring semantic similarity among GO terms and gene products , 2010, Bioinform..

[44]  Aaron R. Quinlan,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[45]  B. Mueller‐Roeber,et al.  Genome-Wide Phylogenetic Comparative Analysis of Plant Transcriptional Regulation: A Timeline of Loss, Gain, Expansion, and Correlation with Complexity , 2010, Genome biology and evolution.

[46]  M. Pellegrini,et al.  Evolution of an Expanded Sex-Determining Locus in Volvox , 2010, Science.

[47]  R. O’Hara,et al.  Female-biased expression on the X chromosome as a key step in sex chromosome evolution in threespine sticklebacks. , 2010, Molecular biology and evolution.

[48]  Evgeny M. Zdobnov,et al.  The Newick utilities: high-throughput phylogenetic tree processing in the Unix shell , 2010, Bioinform..

[49]  D. Filatov,et al.  Plant Y Chromosome Degeneration Is Retarded by Haploid Purifying Selection , 2011, Current Biology.

[50]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[51]  T. Flutre,et al.  Considering Transposable Element Diversification in De Novo Annotation Approaches , 2011, PloS one.

[52]  S. Wessler,et al.  The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies , 2011, Proceedings of the National Academy of Sciences.

[53]  Michael S. Barker,et al.  The Selaginella Genome Identifies Genetic Changes Associated with the Evolution of Vascular Plants , 2011, Science.

[54]  M. Kirkpatrick,et al.  Are all sex chromosomes created equal? , 2011, Trends in genetics : TIG.

[55]  Y. van de Peer,et al.  i-ADHoRe 3.0—fast and sensitive detection of genomic homology in extremely large data sets , 2011, Nucleic acids research.

[56]  Zhengwei Zhu,et al.  CD-HIT: accelerated for clustering the next-generation sequencing data , 2012, Bioinform..

[57]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[58]  R. Quatrano,et al.  RECENT GENE‐CAPTURE ON THE UV SEX CHROMOSOMES OF THE MOSS CERATODON PURPUREUS , 2013, Evolution; international journal of organic evolution.

[59]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[60]  K. Katoh,et al.  Improvements in Performance and Usability , 2013 .

[61]  N. Perrin,et al.  SEX‐CHROMOSOME TURNOVERS INDUCED BY DELETERIOUS MUTATION LOAD , 2013, Evolution; international journal of organic evolution.

[62]  J. G. Burleigh,et al.  RECURRENT EVOLUTION OF DIOECY IN BRYOPHYTES , 2013, Evolution; international journal of organic evolution.

[63]  D. Bachtrog,et al.  Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration , 2013, Nature Reviews Genetics.

[64]  Aaron A. Klammer,et al.  Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data , 2013, Nature Methods.

[65]  Susana M. Coelho,et al.  A Haploid System of Sex Determination in the Brown Alga Ectocarpus sp. , 2014, Current Biology.

[66]  B. Laenen,et al.  Extant diversity of bryophytes emerged from successive post-Mesozoic diversification bursts , 2014, Nature Communications.

[67]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[68]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[69]  S. McDaniel,et al.  Meiotic sex ratio variation in natural populations of Ceratodon purpureus (Ditrichaceae). , 2014, American journal of botany.

[70]  H. Quesneville,et al.  PASTEC: An Automatic Transposable Element Classification Tool , 2014, PloS one.

[71]  Michael I. Love,et al.  Differential analysis of count data – the DESeq2 package , 2013 .

[72]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[73]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[74]  D. Bachtrog,et al.  Numerous Transitions of Sex Chromosomes in Diptera , 2015, PLoS biology.

[75]  S. Otto,et al.  The evolution of sex chromosomes in organisms with separate haploid sexes , 2015, Evolution; international journal of organic evolution.

[76]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[77]  Y. Takehana,et al.  Turnover of Sex Chromosomes in Celebensis Group Medaka Fishes , 2015, G3: Genes, Genomes, Genetics.

[78]  R. Quatrano,et al.  De novo assembly and comparative analysis of the Ceratodon purpureus transcriptome , 2015, Molecular ecology resources.

[79]  W. Karłowski,et al.  The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants , 2014, The New phytologist.

[80]  S. Salzberg,et al.  StringTie enables improved reconstruction of a transcriptome from RNA-seq reads , 2015, Nature Biotechnology.

[81]  S. Kelly,et al.  OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy , 2015, Genome Biology.

[82]  Katharina J. Hoff,et al.  BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS , 2016, Bioinform..

[83]  J. Bowman,et al.  Marchantia MpRKD Regulates the Gametophyte-Sporophyte Transition by Keeping Egg Cells Quiescent in the Absence of Fertilization , 2016, Current Biology.

[84]  Neva C. Durand,et al.  Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. , 2016, Cell systems.

[85]  Matthew G. Johnson,et al.  A phylotranscriptomic analysis of gene family expansion and evolution in the largest order of pleurocarpous mosses (Hypnales, Bryophyta). , 2016, Molecular phylogenetics and evolution.

[86]  P. Bork,et al.  ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data , 2016, Molecular biology and evolution.

[87]  Thomas D. Wu,et al.  GMAP and GSNAP for Genomic Sequence Alignment: Enhancements to Speed, Accuracy, and Functionality , 2016, Statistical Genomics.

[88]  Xinyan Liu,et al.  Cloning and functional characterization of a phenolic acid decarboxylase from the liverwort Conocephalum japonicum. , 2016, Biochemical and biophysical research communications.

[89]  D. Charlesworth.  Plant Sex Chromosomes. , 2016, Annual review of plant biology.

[90]  Bernat Gel,et al.  karyoploteR: an R/Bioconductor package to plot customizable genomes displaying arbitrary data , 2017, bioRxiv.

[91]  David K. Smith,et al.  ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data , 2017 .

[92]  A reconstruction of sexual modes throughout animal evolution , 2017, BMC Evolutionary Biology.

[93]  Feng Luo,et al.  MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads , 2017, Nature Methods.

[94]  S. Rensing,et al.  Comprehensive Genome-Wide Classification Reveals That Many Plant-Specific Transcription Factors Evolved in Streptophyte Algae , 2017, Genome biology and evolution.

[95]  Christian R. Boehm,et al.  Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome , 2017, Cell.

[96]  B. Veit.  Faculty Opinions recommendation of Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. , 2018, Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature.

[97]  T. Kocher,et al.  Unusual Diversity of Sex Chromosomes in African Cichlid Fishes , 2018, Genes.

[98]  Yi Guan,et al.  Two Methods for Mapping and Visualizing Associated Data on Phylogeny Using Ggtree. , 2018, Molecular biology and evolution.

[99]  Michael S. Barker,et al.  Fern genomes elucidate land plant evolution and cyanobacterial symbioses , 2018, Nature Plants.

[100]  Anna Lipzen,et al.  The genomic landscape of molecular responses to natural drought stress in Panicum hallii , 2018, Nature Communications.

[101]  S. Schaeffer.  Muller “Elements” in Drosophila: How the Search for the Genetic Basis for Speciation Led to the Birth of Comparative Genomics , 2018, Genetics.

[102]  Mojgan Amirebrahimi,et al.  The Physcomitrella patens gene atlas project: large-scale RNA-seq based expression data. , 2018, The Plant journal : for cell and molecular biology.

[103]  Richard D. Hayes,et al.  The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. , 2018, The Plant journal : for cell and molecular biology.

[104]  J. G. Burleigh,et al.  Assessing the Performance of Ks Plots for Detecting Ancient Whole Genome Duplications , 2018, Genome biology and evolution.

[105]  One Thousand Plant Transcriptomes Initiative.  One thousand plant transcriptomes and the phylogenomics of green plants , 2019 .

[106]  Yves Van de Peer,et al.  wgd—simple command line tools for the analysis of ancient whole-genome duplications , 2018, Bioinform..

[107]  K. Yamato,et al.  Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin , 2019, Current Biology.

[108]  F. Guerrero,et al.  Sex Chromosome Evolution in Muscid Flies , 2019, G3: Genes, Genomes, Genetics.

[109]  S. Kelly,et al.  OrthoFinder: phylogenetic orthology inference for comparative genomics , 2019, Genome Biology.

[110]  K. Yamato,et al.  A cis‐acting bidirectional transcription switch controls sexual dimorphism in the liverwort , 2019, The EMBO journal.

[111]  Kimberly C. Olney,et al.  “Aligning RNA-Seq reads to a sex chromosome complement informed reference genome increases ability to detect sex differences in gene expression” , 2019 .

[112]  Milot Mirdita,et al.  HH-suite3 for fast remote homology detection and deep protein annotation , 2019, BMC Bioinformatics.