Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity.

The Brassicaceae family comprises c. 4000 species including economically important crops and the model plant Arabidopsis thaliana. Despite their importance, the relationships among major lineages in the family remain unresolved, hampering comparative research. Here, we inferred a Brassicaceae phylogeny using newly generated targeted enrichment sequence data of 1827 exons (> 940 000 bases) representing 63 species, as well as sequenced genome data of 16 species, together representing 50 of the 52 currently recognized Brassicaceae tribes. A third of the samples were derived from herbarium material, facilitating broad taxonomic coverage of the family. Six major clades formed successive sister groups to the rest of Brassicaceae. We also recovered strong support for novel relationships among tribes, and resolved the position of 16 taxa previously not assigned to a tribe. The broad utility of these phylogenetic results is illustrated through a comparative investigation of genome-wide expression signatures that distinguish simple from complex leaves in Brassicaceae. Our study provides an easily extendable dataset for further advances in Brassicaceae systematics and a timely higher-level phylogenetic framework for a wide range of comparative studies of multiple traits in an intensively investigated group of plants.

[1]  M. Sherraden,et al.  The “Universal”: , 2021, Russian Composers Abroad.

[2]  B. Faircloth,et al.  Explosive diversification of marine fishes at the Cretaceous–Palaeogene boundary , 2018, Nature Ecology & Evolution.

[3]  B. Faircloth,et al.  Explosive diversification of marine fishes at the Cretaceous–Palaeogene boundary , 2018, Nature Ecology & Evolution.

[4]  Gerard Talavera,et al.  A Comprehensive and Dated Phylogenomic Analysis of Butterflies , 2018, Current Biology.

[5]  J. Doyle,et al.  Targeting legume loci: A comparison of three methods for target enrichment bait design in Leguminosae phylogenomics , 2018, Applications in plant sciences.

[6]  A. Lemmon,et al.  A pilot study applying the plant Anchored Hybrid Enrichment method to New World sages (Salvia subgenus Calosphace; Lamiaceae). , 2017, Molecular phylogenetics and evolution.

[7]  A. Rokas,et al.  Embracing Uncertainty in Reconstructing Early Animal Evolution , 2017, Current Biology.

[8]  M. Beilstein,et al.  Epistatic interactions drive biased gene retention in the face of massive nuclear introgression , 2017 .

[9]  A. Stamatakis,et al.  Quartet-based computations of internode certainty provide accurate and robust measures of phylogenetic incongruence , 2017, bioRxiv.

[10]  J. Pires,et al.  Anatolian origins and diversification of Aethionema, the sister lineage of the core Brassicaceae. , 2017, American journal of botany.

[11]  Stephen A. Smith,et al.  Widespread paleopolyploidy, gene tree conflict, and recalcitrant relationships among the carnivorous Caryophyllales. , 2017, American journal of botany.

[12]  C. Neinhuis,et al.  Recalcitrant deep and shallow nodes in Aristolochia (Aristolochiaceae) illuminated using anchored hybrid enrichment. , 2017, Molecular phylogenetics and evolution.

[13]  Felipe Zapata,et al.  Pairwise comparisons across species are problematic when analyzing functional genomic data , 2018, Proceedings of the National Academy of Sciences.

[14]  M. Tsiantis,et al.  Using mustard genomes to explore the genetic basis of evolutionary change. , 2017, Current opinion in plant biology.

[15]  Michael S. Barker,et al.  Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention , 2017, bioRxiv.

[16]  A. Rokas,et al.  Contentious relationships in phylogenomic studies can be driven by a handful of genes , 2017, Nature Ecology &Evolution.

[17]  Robert Lanfear,et al.  PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. , 2016, Molecular biology and evolution.

[18]  Mark P. Simmons,et al.  Anchored Phylogenomics of Angiosperms I: Assessing the Robustness of Phylogenetic Estimates , 2016, bioRxiv.

[19]  R. Mott,et al.  The Cardamine hirsuta genome offers insight into the evolution of morphological diversity , 2016, Nature Plants.

[20]  Hang Sun,et al.  Molecular phylogeny reveals the non-monophyly of tribe Yinshanieae (Brassicaceae) and description of a new tribe, Hillielleae , 2016, Plant diversity.

[21]  Matthew G. Johnson,et al.  HybPiper: Extracting coding sequence and introns for phylogenetics from high-throughput sequencing reads using target enrichment1 , 2016, Applications in Plant Sciences.

[22]  Jeffrey P. Townsend,et al.  A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing , 2016, Nature.

[23]  W. Frommer,et al.  50 years of Arabidopsis research: highlights and future directions. , 2016, The New phytologist.

[24]  R. Ewing,et al.  Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta , 2015, Genes & development.

[25]  Yang Zhong,et al.  Resolution of Brassicaceae Phylogeny Using Nuclear Genes Uncovers Nested Radiations and Supports Convergent Morphological Evolution , 2015, Molecular biology and evolution.

[26]  M. Koch,et al.  A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History[OPEN] , 2015, Plant Cell.

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

[28]  D. Weigel,et al.  Beyond the thale: comparative genomics and genetics of Arabidopsis relatives , 2015, Nature Reviews Genetics.

[29]  U. Krämer Planting molecular functions in an ecological context with Arabidopsis thaliana , 2015, eLife.

[30]  N. Ori,et al.  Compound leaf development in model plant species. , 2015, Current opinion in plant biology.

[31]  M. Zytnicki,et al.  Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation , 2015, Nature Plants.

[32]  Mark Fishbein,et al.  Hyb-Seq: Combining target enrichment and genome skimming for plant phylogenomics1 , 2014, Applications in plant sciences.

[33]  Seán G. Brady,et al.  Target enrichment of ultraconserved elements from arthropods provides a genomic perspective on relationships among Hymenoptera , 2014, Molecular ecology resources.

[34]  R. Lanfear,et al.  Selecting optimal partitioning schemes for phylogenomic datasets , 2014, BMC Evolutionary Biology.

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

[36]  F. Vuolo,et al.  Leaf Shape Evolution Through Duplication, Regulatory Diversification, and Loss of a Homeobox Gene , 2014, Science.

[37]  Burke,et al.  A target enrichment method for gathering phylogenetic information from hundreds of loci: An example from the Compositae1 , 2014, Applications in Plant Sciences.

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

[39]  T. Struck,et al.  TreSpEx—Detection of Misleading Signal in Phylogenetic Reconstructions Based on Tree Information , 2014, Evolutionary bioinformatics online.

[40]  A. Lemmon,et al.  High-Throughput Genomic Data in Systematics and Phylogenetics , 2013 .

[41]  D. Hillis,et al.  Targeted Enrichment: Maximizing Orthologous Gene Comparisons across Deep Evolutionary Time , 2013, PloS one.

[42]  I. Al‐Shehbaz A generic and tribal synopsis of the Brassicaceae (Cruciferae) , 2012 .

[43]  R. Tibshirani,et al.  Normalization, testing, and false discovery rate estimation for RNA-sequencing data. , 2012, Biostatistics.

[44]  Christopher A. Miller,et al.  VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. , 2012, Genome research.

[45]  Krzysztof Giaro,et al.  TreeCmp: Comparison of Trees in Polynomial Time , 2012, Evolutionary Bioinformatics Online.

[46]  Frédéric Delsuc,et al.  MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons , 2011, PloS one.

[47]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[48]  D. Weigel,et al.  Developmental genetics and new sequencing technologies: the rise of nonmodel organisms. , 2011, Developmental cell.

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

[50]  A. Liston,et al.  Building a model: developing genomic resources for common milkweed (Asclepias syriaca) with low coverage genome sequencing , 2011, BMC Genomics.

[51]  Eric H. Davidson,et al.  Evolution of Gene Regulatory Networks Controlling Body Plan Development , 2011, Cell.

[52]  I. Al‐Shehbaz,et al.  Cabbage family affairs: the evolutionary history of Brassicaceae. , 2011, Trends in plant science.

[53]  S. Koren,et al.  Assembly algorithms for next-generation sequencing data. , 2010, Genomics.

[54]  S. Warwick,et al.  Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region , 2010, Plant Systematics and Evolution.

[55]  Yue Xiong,et al.  CRL4s: the CUL4-RING E3 ubiquitin ligases. , 2009, Trends in biochemical sciences.

[56]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[57]  E. Kellogg,et al.  Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: tribes and trichomes revisited. , 2008, American journal of botany.

[58]  Miltos Tsiantis,et al.  A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta , 2008, Nature Genetics.

[59]  D. Hillis,et al.  Taxon sampling and the accuracy of phylogenetic analyses , 2008 .

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

[61]  Charles James Nice Bailey,et al.  Toward a global phylogeny of the Brassicaceae. , 2006, Molecular biology and evolution.

[62]  E. Kellogg,et al.  Brassicaceae phylogeny and trichome evolution. , 2006, American journal of botany.

[63]  Kevin P. Byrne,et al.  Rate asymmetry after genome duplication causes substantial long-branch attraction artifacts in the phylogeny of Saccharomyces species. , 2006, Molecular biology and evolution.

[64]  A. King,et al.  Phylogenetic Comparative Analysis: A Modeling Approach for Adaptive Evolution , 2004, The American Naturalist.

[65]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[66]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[67]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

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

[69]  Masami Hasegawa,et al.  CONSEL: for assessing the confidence of phylogenetic tree selection , 2001, Bioinform..

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

[71]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[72]  D. A. German,et al.  Shehbazia (Shehbazieae, Cruciferae), a new monotypic genus and tribe of hybrid origin from Tibet Shehbazia (Shehbazieae, Cruciferae) - новый монотипный род и триба гибридного происхождения из Тибета , 2014 .

[73]  Rasmus Nielsen,et al.  Modeling gene expression evolution with an extended Ornstein-Uhlenbeck process accounting for within-species variation. , 2014, Molecular biology and evolution.

[74]  A. Stamatakis,et al.  BrassiBase: introduction to a novel knowledge database on Brassicaceae evolution. , 2014, Plant & cell physiology.

[75]  Jonathan F. Wendel,et al.  Phylogenetic Incongruence: Window into Genome History and Molecular Evolution , 1998 .