Helitron distribution in Brassicaceae and whole Genome Helitron density as a character for distinguishing plant species

BackgroundHelitron is a rolling-circle DNA transposon; it plays an important role in plant evolution. However, Helitron distribution and contribution to evolution at the family level have not been previously investigated.ResultsWe developed the software easy-to-annotate Helitron (EAHelitron), a Unix-like command line, and used it to identify Helitrons in a wide range of 53 plant genomes (including 13 Brassicaceae species). We determined Helitron density (abundance/Mb) and visualized and examined Helitron distribution patterns. We identified more than 104,653 Helitrons, including many new Helitrons not predicted by other software. Whole genome Helitron density is independent from genome size and shows stability at the species level. Using linear discriminant analysis, de novo genomes (next-generation sequencing) were successfully classified into Arabidopsis thaliana groups. For most Brassicaceae species, Helitron density negatively correlated with gene density, and Helitron distribution patterns were similar to those of A. thaliana. They preferentially inserted into sequence around the centromere and intergenic region. We also associated 13 Helitron polymorphism loci with flowering-time phenotypes in 18 A. thaliana ecotypes.ConclusionEAHelitron is a fast and efficient tool to identify new Helitrons. Whole genome Helitron density can be an informative character for plant classification. Helitron insertion polymorphism could be used in association analysis.

[1]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[2]  S. Wessler,et al.  Treasures in the attic: Rolling circle transposons discovered in eukaryotic genomes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Wayne E. Clarke,et al.  Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea , 2014, Genome Biology.

[4]  Elizabeth A. Kellogg,et al.  An ordinal classification for the families of flowering plants , 1998 .

[5]  Simon M Dittami,et al.  Genomes of extremophile crucifers: new platforms for comparative genomics and beyond , 2012, Genome Biology.

[6]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[7]  Brian D. Ripley,et al.  Modern Applied Statistics with S Fourth edition , 2002 .

[8]  Chunguang Du,et al.  HelitronScanner uncovers a large overlooked cache of Helitron transposons in many plant genomes , 2014, Proceedings of the National Academy of Sciences.

[9]  H. Dooner,et al.  Excision of Helitron Transposons in Maize , 2009, Genetics.

[10]  Andreas Wagner,et al.  The predominantly selfing plant Arabidopsis thaliana experienced a recent reduction in transposable element abundance compared to its outcrossing relative Arabidopsis lyrata , 2012, Mobile DNA.

[11]  Yan Zhang,et al.  A Large Insertion in bHLH Transcription Factor BrTT8 Resulting in Yellow Seed Coat in Brassica rapa , 2012, PloS one.

[12]  Frédéric Bouché,et al.  FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana , 2015, Nucleic Acids Res..

[13]  J. Jurka,et al.  Rolling-circle transposons in eukaryotes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Philippe Bardou,et al.  jvenn: an interactive Venn diagram viewer , 2014, BMC Bioinformatics.

[15]  Chunguang Du,et al.  Rolling-circle amplification of centromeric Helitrons in plant genomes. , 2016, The Plant journal : for cell and molecular biology.

[16]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[17]  Shigeru Iida,et al.  Spontaneous mutations caused by a Helitron transposon, Hel-It1, in morning glory, Ipomoea tricolor. , 2007, The Plant journal : for cell and molecular biology.

[18]  Sean R. Eddy,et al.  Pack-MULE transposable elements mediate gene evolution in plants , 2004, Nature.

[19]  Olga Golosova,et al.  Unipro UGENE: a unified bioinformatics toolkit , 2012, Bioinform..

[20]  Yehua He,et al.  TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface , 2018 .

[21]  S Wright,et al.  Transposon diversity in Arabidopsis thaliana. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Jurka,et al.  Molecular paleontology of transposable elements from Arabidopsis thaliana. , 1999 .

[23]  J. Bennetzen,et al.  Structure-based discovery and description of plant and animal Helitrons , 2009, Proceedings of the National Academy of Sciences.

[24]  Brandon S Gaut,et al.  Population and evolutionary dynamics of Helitron transposable elements in Arabidopsis thaliana. , 2007, Molecular biology and evolution.

[25]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[26]  Hongya Gu,et al.  Constitutive expression of CIR1 (RVE2) affects several circadian-regulated processes and seed germination in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[27]  Bing Li,et al.  Helitron-like transposons contributed to the mating system transition from out-crossing to self-fertilizing in polyploid Brassica napus L. , 2016, Scientific Reports.

[28]  M. Morgante,et al.  Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize , 2005, Nature Genetics.

[29]  Noah A. Rosenberg,et al.  Demographic History of European Populations of Arabidopsis thaliana , 2008, PLoS genetics.

[30]  Corinne Da Silva,et al.  Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome , 2014, Science.

[31]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

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

[33]  Andreas Gogol-Döring,et al.  A Helitron transposon reconstructed from bats reveals a novel mechanism of genome shuffling in eukaryotes , 2016, Nature Communications.

[34]  Richard M. Clark,et al.  The Arabidopsis lyrata genome sequence and the basis of rapid genome size change , 2011, Nature Genetics.

[35]  Hadi Quesneville,et al.  Understanding Brassicaceae evolution through ancestral genome reconstruction , 2015, Genome Biology.

[36]  Christian Biémont,et al.  Genetics: Junk DNA as an evolutionary force , 2006, Nature.

[37]  S. Wright,et al.  Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. , 2003, Genome research.

[38]  Chengjie Chen,et al.  TBtools, a Toolkit for Biologists integrating various HTS-data handling tools with a user-friendly interface , 2018, bioRxiv.

[39]  B. Mcclintock.  The origin and behavior of mutable loci in maize , 1950, Proceedings of the National Academy of Sciences.

[40]  Lin Fang,et al.  WEGO: a web tool for plotting GO annotations , 2006, Nucleic Acids Res..

[41]  Lila Vodkin,et al.  Novel exon combinations generated by alternative splicing of gene fragments mobilized by a CACTA transposon in Glycine max , 2007, BMC Plant Biology.

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

[43]  J. Lundberg,et al.  An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants : APG II THE ANGIOSPERM PHYLOGENY GROUP * , 2003 .

[44]  Lincoln Stein,et al.  Using GBrowse 2.0 to visualize and share next-generation sequence data , 2013, Briefings Bioinform..

[45]  Kurt Hornik,et al.  Introduction to arules – A computational environment for mining association rules and frequent item sets , 2009 .

[46]  He Zhang,et al.  The high‐quality genome of Brassica napus cultivar ‘ZS11’ reveals the introgression history in semi‐winter morphotype , 2017, The Plant journal : for cell and molecular biology.

[47]  Vipin T. Sreedharan,et al.  Multiple reference genomes and transcriptomes for Arabidopsis thaliana , 2011, Nature.

[48]  Rodrigo Lopez,et al.  WU-Blast2 server at the European Bioinformatics Institute , 2003, Nucleic Acids Res..

[49]  Lior Pachter,et al.  VISTA: computational tools for comparative genomics , 2004, Nucleic Acids Res..

[50]  Ben C. Stöver,et al.  TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses , 2010, BMC Bioinformatics.

[51]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[52]  Helga Thorvaldsdóttir,et al.  Integrative Genomics Viewer , 2011, Nature Biotechnology.

[53]  Nam-Soo Kim,et al.  The genomes and transposable elements in plants: are they friends or foes? , 2017, Genes & Genomics.

[54]  Nansheng Chen,et al.  Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences , 2009, Current protocols in bioinformatics.

[55]  Jian Wang,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.

[56]  L. Stein,et al.  JBrowse: a next-generation genome browser. , 2009, Genome research.

[57]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[58]  Chentao Lin,et al.  Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis , 2008, Science.

[59]  Vladimir V. Kapitonov,et al.  Molecular paleontology of transposable elements from Arabidopsis thaliana , 2004, Genetica.

[60]  Jerzy Jurka,et al.  Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor , 2006, BMC Bioinformatics.

[61]  Jason S. Caronna,et al.  Computational prediction and molecular confirmation of Helitron transposons in the maize genome , 2008, BMC Genomics.

[62]  W. Belknap,et al.  Characterization of Repetitive DNA Elements in Arabidopsis , 1999, Journal of Molecular Evolution.

[63]  Lixing Yang,et al.  Distribution, diversity, evolution, and survival of Helitrons in the maize genome , 2009, Proceedings of the National Academy of Sciences.

[64]  J. Poulain,et al.  The genome of the mesopolyploid crop species Brassica rapa , 2011, Nature Genetics.

[65]  Andy South,et al.  rworldmap : a new R package for mapping global data , 2011, R J..

[66]  Hilde van der Togt,et al.  Publisher's Note , 2003, J. Netw. Comput. Appl..

[67]  Kun Lu,et al.  The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes , 2014, Nature Communications.