The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution

Daniel Lang, Kristian K. Ullrich, Florent Murat, Jörg Fuchs, Jerry Jenkins, Fabian B. Haas, Mathieu Piednoel, Heidrun Gundlach, Michiel Van Bel, Rabea Meyberg, Cristina Vives, Jordi Morata, Aikaterini Symeonidi, Manuel Hiss, Wellington Muchero, Yasuko Kamisugi, Omar Saleh, Guillaume Blanc, Eva L. Decker, Nico van GesselJane Grimwood, Richard D. Hayes, Sean W. Graham, Lee E. Gunter, Stuart F. McDaniel, Sebastian N.W. Hoernstein, Anders Larsson, Fay Wei Li, Pierre François Perroud, Jeremy Phillips, Priya Ranjan, Daniel S. Rokshar, Carl J. Rothfels, Lucas Schneider, Shengqiang Shu, Dennis W. Stevenson, Fritz Thümmler, Michael Tillich, Juan C. Villarreal Aguilar, Thomas Widiez, Gane Ka Shu Wong, Ann Wymore, Yong Zhang, Andreas D. Zimmer, Ralph S. Quatrano, Klaus F.X. Mayer, David Goodstein, Josep M. Casacuberta, Klaas Vandepoele, Ralf Reski, Andrew C. Cuming, Gerald A. Tuskan, Florian Maumus, Jérome Salse, Jeremy Schmutz, Stefan A. Rensing

Research output: Contribution to journalArticlepeer-review

300 Scopus citations

Abstract

The draft genome of the moss model, Physcomitrella patens, comprised approximately 2000 unordered scaffolds. In order to enable analyses of genome structure and evolution we generated a chromosome-scale genome assembly using genetic linkage as well as (end) sequencing of long DNA fragments. We find that 57% of the genome comprises transposable elements (TEs), some of which may be actively transposing during the life cycle. Unlike in flowering plant genomes, gene- and TE-rich regions show an overall even distribution along the chromosomes. However, the chromosomes are mono-centric with peaks of a class of Copia elements potentially coinciding with centromeres. Gene body methylation is evident in 5.7% of the protein-coding genes, typically coinciding with low GC and low expression. Some giant virus insertions are transcriptionally active and might protect gametes from viral infection via siRNA mediated silencing. Structure-based detection methods show that the genome evolved via two rounds of whole genome duplications (WGDs), apparently common in mosses but not in liverworts and hornworts. Several hundred genes are present in colinear regions conserved since the last common ancestor of plants. These syntenic regions are enriched for functions related to plant-specific cell growth and tissue organization. The P. patens genome lacks the TE-rich pericentromeric and gene-rich distal regions typical for most flowering plant genomes. More non-seed plant genomes are needed to unravel how plant genomes evolve, and to understand whether the P. patens genome structure is typical for mosses or bryophytes.

Original languageEnglish
Pages (from-to)515-533
Number of pages19
JournalPlant Journal
Volume93
Issue number3
DOIs
StatePublished - Feb 1 2018

Funding

We thank Richard Haas, Faezeh Donges, Marco Go\u20ACttig and Katrin Kumke for technical assistance. We thank Walter Sanseverino and Riccardo Aliese (Sequentia Biotech) for assistance in TE RNAseq analyses. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. Support to RR and SAR by the German Research Foundation (DFG RE 837/10-2), the Excellence Initiative of the German Federal and State Governments (EXC 294), and by the German Federal Ministry of Education and Research (BMBF FRISYS), is highly appreciated. CoGe is supported by the US National Science Foundation under Award Numbers IOS-339156 and IOS-1444490, CyVerse is supported by the U.S. National Science Foundation under Award Numbers DBI-0735191 and DBI-1265383. YK and ACC are grateful for support from the UK Biological Sciences and Biotechnology Research Council (Grant BB/F001797/1). KV acknowledges the Multidisciplinary Research Partnership \u2018Bioinformatics: from nucleotides to networks\u2019 Project (no 01MR0410W) of Ghent University. JC is grateful for support from the Spanish Ministerio de Econom\u00EDa y Competitividad (Grant AGL2013-43244-R). RSQ is grateful to Monsanto (St. Louis, MO, USA) for sequencing genomic DNA of P. patens accession Kaskaskia. The 1000 Plants (1 KP) initiative, led by GKSW, is funded by the Alberta Ministry of Innovation and Advanced Education, Alberta Innovates Technology Futures (AITF), Innovates Centres of Research Excellence (iCORE), Musea Ventures, BGI-Shenzhen and China National Genebank (CNGB). TW was supported by EMBO Long-Term Fellowships (ALTF 1166-2011) and by Marie Curie Actions (European Commission EMBOCOFUND2010, GA-2010-267146). The work conducted at PGSB was supported by the German Research Foundation (SFB924) and German Ministry of Education and Research (BMBF, 031A536/ de.NBI). The authors declare that they have no competing interests.

Keywords

  • Physcomitrella patens
  • chromosome
  • duplication
  • evolution
  • genome
  • methylation
  • moss
  • plant
  • synteny

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