Transposable elements contribute to dynamic genome content in maize

Transposable elements (TEs) are ubiquitous components of eukaryotic genomes and can create variation in genomic organization. The majority of maize genomes are composed of TEs. We developed an approach to define shared and variable TE insertions across genome assemblies and applied this method to four maize genomes (B73, W22, Mo17, and PH207). Among these genomes we identified 1.6 Gb of variable TE sequence representing a combination of recent TE movement and deletion of previously existing TEs. Although recent TE movement only accounted for a portion of the TE variability, we identified 4,737 TEs unique to one genome with defined insertion sites in all other genomes. Variable TEs are found for all superfamilies and are distributed across the genome, including in regions of recent shared ancestry among individuals. There are 2,380 genes annotated in the B73 genome located within variable TEs, providing evidence for the role of TEs in contributing to the substantial differences in gene content among these genotypes. The large scope of TE variation present in this limited sample of temperate maize genomes highlights the major contribution of TEs in driving variation in genome organization and gene content. Significance Statement The majority of the maize genome is comprised of transposable elements (TEs) that have the potential to create genomic variation within species. We developed a method to identify shared and non-shared TEs using whole genome assemblies of four maize inbred lines. Variable TEs are found throughout the maize genome and in comparisons of any two genomes we find ~20% of the genome is due to non-shared TEs. Several thousand maize genes are found within TEs that are variable across lines, highlighting the contribution of TEs to gene content variation. This study creates a comprehensive resource for genomic studies of TE variability among four maize genomes, which will enable studies on the consequences of variable TEs on genome function.

[1]  Gene Family , 2020, Definitions.

[2]  Nathan M. Springer,et al.  Dynamic Patterns of Transcript Abundance of Transposable Element Families in Maize , 2019, G3: Genes, Genomes, Genetics.

[3]  H. Dooner,et al.  Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions , 2019, Proceedings of the National Academy of Sciences.

[4]  X. Gu,et al.  TIR-Learner, a New Ensemble Method for TIR Transposable Element Annotation, Provides Evidence for Abundant New Transposable Elements in the Maize Genome. , 2019, Molecular plant.

[5]  Nathan M. Springer,et al.  The genomic ecosystem of transposable elements in maize , 2019, bioRxiv.

[6]  O. Panaud,et al.  Retrotranspositional landscape of Asian rice revealed by 3000 genomes , 2019, Nature Communications.

[7]  Daniel L. Vera,et al.  The maize W22 genome provides a foundation for functional genomics and transposon biology , 2018, Nature Genetics.

[8]  P. Schnable,et al.  Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes , 2018, Nature Genetics.

[9]  Gregory J. Zynda,et al.  Subtle Perturbations of the Maize Methylome Reveal Genes and Transposons Silenced by Chromomethylase or RNA-Directed DNA Methylation Pathways , 2018, G3: Genes, Genomes, Genetics.

[10]  Alain Charcosset,et al.  Sequence analysis of European maize inbred line F2 provides new insights into molecular and chromosomal characteristics of presence/absence variants , 2018, BMC Genomics.

[11]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[12]  Alex B. Brohammer,et al.  Limited role of differential fractionation in genome content variation and function in maize (Zea mays L.) inbred lines , 2017, bioRxiv.

[13]  W. Jin,et al.  ZmCCT9 enhances maize adaptation to higher latitudes , 2017, Proceedings of the National Academy of Sciences.

[14]  Gregory J. Zynda,et al.  Subtle perturbations of the maize methylome reveal genes and transposons silenced by DNA methylation , 2017, bioRxiv.

[15]  Gengyun Zhang,et al.  Genome-wide characterization of non-reference transposable element insertion polymorphisms reveals genetic diversity in tropical and temperate maize , 2017, BMC Genomics.

[16]  C. Feschotte,et al.  Regulatory activities of transposable elements: from conflicts to benefits , 2016, Nature Reviews Genetics.

[17]  Kevin L. Schneider,et al.  Improved maize reference genome with single-molecule technologies , 2017, Nature.

[18]  Nathan M. Springer,et al.  Transposable element influences on gene expression in plants. , 2017, Biochimica et biophysica acta. Gene regulatory mechanisms.

[19]  Kevin L. Childs,et al.  Draft Assembly of Elite Inbred Line PH207 Provides Insights into Genomic and Transcriptome Diversity in Maize[OPEN] , 2016, Plant Cell.

[20]  Ben Nichols,et al.  Distributed under Creative Commons Cc-by 4.0 Vsearch: a Versatile Open Source Tool for Metagenomics , 2022 .

[21]  James C. Schnable,et al.  Integration of omic networks in a developmental atlas of maize , 2016, Science.

[22]  G. Mayhew,et al.  The Arabidopsis thaliana mobilome and its impact at the species level , 2016, eLife.

[23]  Yuliya V. Karpievitch,et al.  Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation , 2016, bioRxiv.

[24]  Samuel Müller,et al.  Fast and flexible methods for monotone polynomial fitting , 2016 .

[25]  Patricia P. Chan,et al.  GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes , 2015, Nucleic Acids Res..

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

[27]  R. Dawe,et al.  Genetic and Genomic Toolbox of Zea mays , 2015, Genetics.

[28]  Peter J. Bradbury,et al.  Joint-multiple family linkage analysis predicts within-family variation better than single-family analysis of the maize nested association mapping population , 2015, Heredity.

[29]  Xiekui Cui,et al.  Epigenetic regulation and functional exaptation of transposable elements in higher plants. , 2014, Current opinion in plant biology.

[30]  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.

[31]  M. Mirouze,et al.  Transposable elements, a treasure trove to decipher epigenetic variation: insights from Arabidopsis and crop epigenomes. , 2014, Journal of experimental botany.

[32]  J. Bennetzen,et al.  The contributions of transposable elements to the structure, function, and evolution of plant genomes. , 2014, Annual review of plant biology.

[33]  M. Pindo,et al.  A MITE Transposon Insertion Is Associated with Differential Methylation at the Maize Flowering Time QTL Vgt1 , 2014, G3: Genes, Genomes, Genetics.

[34]  M. A. Pedraza,et al.  Insights into the Maize Pan-Genome and Pan-Transcriptome[W][OPEN] , 2014, Plant Cell.

[35]  Xiaohong Yang,et al.  CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize , 2013, Proceedings of the National Academy of Sciences.

[36]  T. Richmond,et al.  Changes in genome content generated via segregation of non-allelic homologs. , 2012, The Plant journal : for cell and molecular biology.

[37]  S. Cannon,et al.  Genome-Wide Characterization of Nonreference Transposons Reveals Evolutionary Propensities of Transposons in Soybean[C][W] , 2012, Plant Cell.

[38]  Douglas R. Hoen,et al.  A Gene Family Derived from Transposable Elements during Early Angiosperm Evolution Has Reproductive Fitness Benefits in Arabidopsis thaliana , 2012, PLoS genetics.

[39]  Peter J. Bradbury,et al.  Maize HapMap2 identifies extant variation from a genome in flux , 2012, Nature Genetics.

[40]  Xun Xu,et al.  Comparative population genomics of maize domestication and improvement , 2012, Nature Genetics.

[41]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[42]  T. Zerjal,et al.  Maize genetic diversity and association mapping using transposable element insertion polymorphisms , 2012, Theoretical and Applied Genetics.

[43]  R. Slotkin,et al.  Gene Expression and Stress Response Mediated by the Epigenetic Regulation of a Transposable Element Small RNA , 2012, PLoS genetics.

[44]  Damon Lisch,et al.  How important are transposons for plant evolution? , 2012, Nature Reviews Genetics.

[45]  Jeffrey Ross-Ibarra,et al.  Identification of a functional transposon insertion in the maize domestication gene tb1 , 2011, Nature Genetics.

[46]  Heng Li,et al.  A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data , 2011, Bioinform..

[47]  Bernd Weisshaar,et al.  Targeted Identification of Short Interspersed Nuclear Element Families Shows Their Widespread Existence and Extreme Heterogeneity in Plant Genomes[W] , 2011, Plant Cell.

[48]  M. Frith,et al.  Adaptive seeds tame genomic sequence comparison. , 2011, Genome research.

[49]  James C. Schnable,et al.  Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss , 2011, Proceedings of the National Academy of Sciences.

[50]  José M. Sempere,et al.  The Gypsy Database (GyDB) of mobile genetic elements: release 2.0 , 2010, Nucleic Acids Res..

[51]  Jian Wang,et al.  Genome-wide patterns of genetic variation among elite maize inbred lines , 2010, Nature Genetics.

[52]  Peter Tiffin,et al.  Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. , 2010, Genome research.

[53]  V. Brendel,et al.  Genome-Wide Distribution of Transposed Dissociation Elements in Maize[W][OA] , 2010, Plant Cell.

[54]  James C. Schnable,et al.  Following Tetraploidy in Maize, a Short Deletion Mechanism Removed Genes Preferentially from One of the Two Homeologs , 2010, PLoS biology.

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

[56]  Richard Durbin,et al.  Fast and accurate long-read alignment with Burrows–Wheeler transform , 2010, Bioinform..

[57]  Chunguang Du,et al.  The polychromatic Helitron landscape of the maize genome , 2009, Proceedings of the National Academy of Sciences.

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

[59]  Patrick S. Schnable,et al.  Maize Inbreds Exhibit High Levels of Copy Number Variation (CNV) and Presence/Absence Variation (PAV) in Genome Content , 2009, PLoS genetics.

[60]  Cristian Chaparro,et al.  Exceptional Diversity, Non-Random Distribution, and Rapid Evolution of Retroelements in the B73 Maize Genome , 2009, PLoS genetics.

[61]  S. Kurtz,et al.  Fine-grained annotation and classification of de novo predicted LTR retrotransposons , 2009, Nucleic acids research.

[62]  Wei Li,et al.  BSMAP: whole genome bisulfite sequence MAPping program , 2009, BMC Bioinformatics.

[63]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[64]  S. Wessler,et al.  TARGeT: a web-based pipeline for retrieving and characterizing gene and transposable element families from genomic sequences , 2009, Nucleic Acids Research.

[65]  Michael Freeling,et al.  The Value of Nonmodel Genomes and an Example Using SynMap Within CoGe to Dissect the Hexaploidy that Predates the Rosids , 2008, Tropical Plant Biology.

[66]  Xuehui Huang,et al.  Genome-Wide Analysis of Transposon Insertion Polymorphisms Reveals Intraspecific Variation in Cultivated Rice1[W][OA] , 2008, Plant Physiology.

[67]  S. Hake,et al.  The art and design of genetic screens: maize , 2008, Nature Reviews Genetics.

[68]  Stefan Kurtz,et al.  LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons , 2008, BMC Bioinformatics.

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

[70]  Robert S. Harris Improved Pairwise Alignmnet of Genomic DNA , 2007 .

[71]  H. Dooner,et al.  Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus , 2006, Proceedings of the National Academy of Sciences.

[72]  J. Bennetzen,et al.  Transposable elements, gene creation and genome rearrangement in flowering plants. , 2005, Current opinion in genetics & development.

[73]  Richard M. Clark,et al.  Estimating a nucleotide substitution rate for maize from polymorphism at a major domestication locus. , 2005, Molecular biology and evolution.

[74]  K. Koch,et al.  Steady-state transposon mutagenesis in inbred maize. , 2005, The Plant journal : for cell and molecular biology.

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

[76]  Joachim Messing,et al.  Gene movement by Helitron transposons contributes to the haplotype variability of maize. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Michele Morgante,et al.  Evolution of DNA Sequence Nonhomologies among Maize Inbredsw⃞ , 2005, The Plant Cell Online.

[78]  Steven Salzberg,et al.  DAGchainer: a tool for mining segmental genome duplications and synteny , 2004, Bioinform..

[79]  Jianxin Ma,et al.  Close split of sorghum and maize genome progenitors. , 2004, Genome research.

[80]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[81]  T. Brutnell,et al.  Transposon tagging using Activator (Ac) in maize. , 2003, Methods in molecular biology.

[82]  H. Fu,et al.  Intraspecific violation of genetic colinearity and its implications in maize , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[83]  P. Schnable,et al.  Molecular characterization of meiotic recombination across the 140-kb multigenic a1-sh2 interval of maize , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[85]  S. Wessler,et al.  Recent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[86]  M. Van Montagu,et al.  Transposon Display identifies individual transposable elements in high copy number lines. , 2002, The Plant journal : for cell and molecular biology.

[87]  J. Bennetzen,et al.  Do Plants Have a One-Way Ticket to Genomic Obesity? , 1997, The Plant cell.

[88]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[89]  J. Bennetzen,et al.  Nested Retrotransposons in the Intergenic Regions of the Maize Genome , 1996, Science.

[90]  S. Wessler,et al.  Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. , 1992, The Plant cell.

[91]  Wen-Hsiung Li,et al.  Evolution of DNA Sequences , 1985 .

[92]  B. Mcclintock,et al.  The significance of responses of the genome to challenge. , 1984, Science.

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