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

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

doi:10.1111/tpj.13801

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

Journal Article · Tue Dec 12 19:00:00 EST 2017 · The Plant Journal

DOI: https://doi.org/10.1111/tpj.13801 · OSTI ID:1439140

^[1];

^[2]; Murat, Florent ^[3]; Fuchs, Jorg ^[4]; Jenkins, Jerry ^[5];

^[2]; Piednoel, Mathieu ^[6]; Gundlach, Heidrun ^[7]; Van Bel, Michiel ^[8]; Meyberg, Rabea ^[2]; Vives, Cristina ^[9]; Morata, Jordi ^[9]; Symeonidi, Aikaterini ^[2]; Hiss, Manuel ^[2]; Muchero, Wellington ^[10];

^[11]; Saleh, Omar ^[12]; Blanc, Guillaume ^[13]; Decker, Eva L. ^[12]; van Gessel, Nico ^[12] more »

Univ. of Freiburg, Freiburg (Germany); Helmholtz Center Munich, Neuherberg (Germany)
Univ. of Marburg, Marburg (Germany)
UMR 1095 Genetics, Diversity and Ecophysiology of Cereals (GDEC), Clermont-Ferrand (France)
Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Stadt Seeland (Germany)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
Max Planck Institute for Plant Breeding Research, Cologne (Germany)
Helmholtz Center Munich, Neuherberg (Germany)
VIB Center for Plant Systems Biology, Ghent (Belgium); Ghent Univ., Ghent (Belgium)
Center for Research in Agricultural Genomics, CRAG (CSIC-IRTA-UAB-UB), Barcelona (Spain)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Leeds, Leeds (United Kingdom)
Univ. of Freiburg, Freiburg (Germany)
Aix-Marseille Univ., Marseille (France)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of British Columbia, Vancouver, BC (Canada)
Univ. of Florida, Gainesville, FL (United States)
Uppsala Univ., Uppsala (Sweden)
Boyce Thompson Institute, Ithaca, NY (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States)
New York Botanical Garden, Bronx, NY (United States)
Vertis Biotechnologie AG, Freising (Germany)
Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm (Germany)
Univ. Laval, QC (Canada)
Univ. of Geneva, Geneva (Switzerland); Rutgers Univ., New Brunswick, NJ (United States)
Univ. of AlbertaEdmonton, AB (Canada); BGI-Shenzhen, Yantian District Shenzhen (China)
Shenzhen Huahan Gene Life Technology Co. Ltd, Shenzhen (China)
Washington Univ., St. Louis, MO (United States)
Helmholtz Center Munich, Neuherberg (Germany); WZW, Technical Univ. Munich, Munich (Germany)
Univ. Paris-Saclay, Versailles (France)
INRA, Clermont-Ferrand (France)
Univ. of Marburg, Marburg (Germany); Univ. of Freiburg, Freiburg (Germany)

Here, 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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1439140

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Journal Issue: 3 Vol. 93; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Engineering modular diterpene biosynthetic pathways in Physcomitrella patens Banerjee, Aparajita; Arnesen, Jonathan A.; Moser, Daniel Planta, Vol. 249, Issue 1 https://doi.org/10.1007/s00425-018-3053-0	journal	November 2018
RdDM-independent de novo and heterochromatin DNA methylation by plant CMT and DNMT3 orthologs Yaari, Rafael; Katz, Aviva; Domb, Katherine Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09496-0	journal	April 2019
The hornwort genome and early land plant evolution Zhang, Jian; Fu, Xin-Xing; Li, Rui-Qi Nature Plants, Vol. 6, Issue 2 https://doi.org/10.1038/s41477-019-0588-4	journal	February 2020
Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts Li, Fay-Wei; Nishiyama, Tomoaki; Waller, Manuel Nature Plants, Vol. 6, Issue 3 https://doi.org/10.1038/s41477-020-0618-2	journal	March 2020
Cytological analysis and structural quantification of FtsZ1-2 and FtsZ2-1 network characteristics in Physcomitrella patens Özdemir, Bugra; Asgharzadeh, Pouyan; Birkhold, Annette I. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-29284-y	journal	July 2018
Unique Molecular Identifiers reveal a novel sequencing artefact with implications for RNA-Seq based gene expression analysis Sena, Johnny A.; Galotto, Giulia; Devitt, Nico P. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-31064-7	journal	September 2018
The gynoecious CmWIP1 transcription factor interacts with CmbZIP48 to inhibit carpel development Eleblu, John S. Y.; Haraghi, Aimen; Mania, Brahim Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-52004-z	journal	October 2019
The C-Fern (Ceratopteris richardii) genome: insights into plant genome evolution with the first partial homosporous fern genome assembly Marchant, D. Blaine; Sessa, Emily B.; Wolf, Paul G. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53968-8	journal	December 2019
Ancient duplications and grass-specific transposition influenced the evolution of LEAFY transcription factor genes Gao, Bei; Chen, Moxian; Li, Xiaoshuang Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0469-4	journal	June 2019
Embryophyte stress signaling evolved in the algal progenitors of land plants de Vries, Jan; Curtis, Bruce A.; Gould, Sven B. Proceedings of the National Academy of Sciences, Vol. 115, Issue 15 https://doi.org/10.1073/pnas.1719230115	journal	March 2018
Light-regulated PAS-containing histidine kinases delay gametophore formation in the moss Physcomitrella patens Ryo, Masashi; Yamashino, Takafumi; Nomoto, Yuji Journal of Experimental Botany, Vol. 69, Issue 20 https://doi.org/10.1093/jxb/ery257	journal	August 2018
Characterization of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model Meyberg, Rabea; Perroud, Pierre-François; Haas, Fabian B. https://doi.org/10.1101/728691	posted_content	August 2019
Chromatin organization in early land plants reveals an ancestral association between H3K27me3, transposons, and constitutive heterochromatin Montgomery, Sean A.; Tanizawa, Yasuhiro; Galik, Bence https://doi.org/10.1101/827881	posted_content	November 2019
Distinct types of short open reading frames are translated in plant cells Fesenko, Igor; Kirov, Ilya; Kniazev, Andrey Genome Research, Vol. 29, Issue 9 https://doi.org/10.1101/gr.253302.119	journal	August 2019
Characterization of spa mutants in the moss Physcomitrella provides evidence for functional divergence of SPA genes during the evolution of land plants Artz, Oliver; Dickopf, Stephen; Ranjan, Aashish New Phytologist, Vol. 224, Issue 4 https://doi.org/10.1111/nph.16004	journal	July 2019
Physcomitrella patens Reute mC herry as a tool for efficient crossing within and between ecotypes Perroud, P. ‐F.; Meyberg, R.; Rensing, S. A. Plant Biology, Vol. 21, Issue S1 https://doi.org/10.1111/plb.12840	journal	May 2018
Roles of RAD 51 and RTEL 1 in telomere and rDNA stability in Physcomitrella patens Goffová, Ivana; Vágnerová, Radka; Peška, Vratislav The Plant Journal https://doi.org/10.1111/tpj.14304	journal	April 2019
Two ANGUSTIFOLIA genes regulate gametophore and sporophyte development in Physcomitrella patens Hashida, Yoshikazu; Takechi, Katsuaki; Abiru, Tomomi The Plant Journal, Vol. 101, Issue 6 https://doi.org/10.1111/tpj.14592	journal	December 2019
A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha Diop, Seydina I.; Subotic, Oliver; Giraldo‐Fonseca, Alejandro The Plant Journal, Vol. 101, Issue 6 https://doi.org/10.1111/tpj.14602	journal	December 2019
PEATmoss ( Physcomitrella Expression Atlas Tool): a unified gene expression atlas for the model plant Physcomitrella patens Fernandez‐Pozo, Noe; Haas, Fabian B.; Meyberg, Rabea The Plant Journal, Vol. 102, Issue 1 https://doi.org/10.1111/tpj.14607	journal	January 2020
Genome-Wide Identification, Evolution, and Transcriptional Profiling of PP2C Gene Family in Brassica rapa Khan, Nadeem; Ke, Han; Hu, Chun-mei BioMed Research International, Vol. 2019 https://doi.org/10.1155/2019/2965035	journal	April 2019
Genome-wide characterization of a SRO gene family involved in response to biotic and abiotic stresses in banana (Musa spp.) Zhang, Lu; Zhou, Dengbo; Hu, Huigang BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1807-x	journal	May 2019
Phylogenomic synteny network analyses reveal ancestral transpositions of auxin response factor genes in plants Gao, Bei; Wang, Liuqiang; Oliver, Melvin Plant Methods, Vol. 16, Issue 1 https://doi.org/10.1186/s13007-020-00609-1	journal	May 2020
Nested plant LTR retrotransposons target specific regions of other elements, while all LTR retrotransposons often target palindromes and nucleosome-occupied regions: in silico study Jedlicka, Pavel; Lexa, Matej; Vanat, Ivan Mobile DNA, Vol. 10, Issue 1 https://doi.org/10.1186/s13100-019-0186-z	journal	December 2019
Genome Sequencing of Pleurozium schreberi : The Assembled and Annotated Draft Genome of a Pleurocarpous Feather Moss Pederson, Eric R. A.; Warshan, Denis; Rasmussen, Ulla G3: Genes\|Genomes\|Genetics, Vol. 9, Issue 9 https://doi.org/10.1534/g3.119.400279	journal	July 2019
Evolution of the Symbiosis-Specific GRAS Regulatory Network in Bryophytes Grosche, Christopher; Genau, Anne Christina; Rensing, Stefan A. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01621	journal	November 2018
Simplified Transformation of Ostreococcus tauri Using Polyethylene Glycol Sanchez, Frédéric; Geffroy, Solène; Norest, Manon Genes, Vol. 10, Issue 5 https://doi.org/10.3390/genes10050399	journal	May 2019
Genome-Wide Analysis of the MYB Transcription Factor Superfamily in Physcomitrella patens Pu, Xiaojun; Yang, Lixin; Liu, Lina International Journal of Molecular Sciences, Vol. 21, Issue 3 https://doi.org/10.3390/ijms21030975	journal	February 2020
Pilot satellitome analysis of the model plant, Physcomitrella patens, revealed a transcribed and high-copy IGS related tandem repeat Kirov, Ilya; Gilyok, Marina; Knyazev, Andrey Comparative Cytogenetics, Vol. 12, Issue 4 https://doi.org/10.3897/compcytogen.v12i4.31015	journal	December 2018

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