Assembly of the Boechera retrofracta Genome and Evolutionary Analysis of Apomixis-Associated Genes
Identifieur interne : 000C93 ( Pmc/Corpus ); précédent : 000C92; suivant : 000C94Assembly of the Boechera retrofracta Genome and Evolutionary Analysis of Apomixis-Associated Genes
Auteurs : Sergei Kliver ; Mike Rayko ; Alexey Komissarov ; Evgeny Bakin ; Daria Zhernakova ; Kasavajhala Prasad ; Catherine Rushworth ; R. Baskar ; Dmitry Smetanin ; Jeremy Schmutz ; Daniel S. Rokhsar ; Thomas Mitchell-Olds ; Ueli Grossniklaus ; Vladimir BrukhinSource :
- Genes [ 2073-4425 ] ; 2018.
Abstract
Closely related to the model plant
Url:
DOI: 10.3390/genes9040185
PubMed: 29597328
PubMed Central: 5924527
Links to Exploration step
PMC:5924527Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Assembly of the <italic>Boechera retrofracta</italic> Genome and Evolutionary Analysis of Apomixis-Associated Genes</title><author><name sortKey="Kliver, Sergei" sort="Kliver, Sergei" uniqKey="Kliver S" first="Sergei" last="Kliver">Sergei Kliver</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation><affiliation><nlm:aff id="af2-genes-09-00185">All-Russia Research Institute for Agricultural Microbiology, Podbelskogo sh. 3, Pushkin, 196608 St. Petersburg, Russia</nlm:aff></affiliation></author><author><name sortKey="Rayko, Mike" sort="Rayko, Mike" uniqKey="Rayko M" first="Mike" last="Rayko">Mike Rayko</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Komissarov, Alexey" sort="Komissarov, Alexey" uniqKey="Komissarov A" first="Alexey" last="Komissarov">Alexey Komissarov</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Bakin, Evgeny" sort="Bakin, Evgeny" uniqKey="Bakin E" first="Evgeny" last="Bakin">Evgeny Bakin</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Zhernakova, Daria" sort="Zhernakova, Daria" uniqKey="Zhernakova D" first="Daria" last="Zhernakova">Daria Zhernakova</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Prasad, Kasavajhala" sort="Prasad, Kasavajhala" uniqKey="Prasad K" first="Kasavajhala" last="Prasad">Kasavajhala Prasad</name><affiliation><nlm:aff id="af3-genes-09-00185">Department of Biology, Colorado State University, Fort Collins, CO 80523; USA;<email>kasavajhalaprasad@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Rushworth, Catherine" sort="Rushworth, Catherine" uniqKey="Rushworth C" first="Catherine" last="Rushworth">Catherine Rushworth</name><affiliation><nlm:aff id="af4-genes-09-00185">University and Jepson Herbaria, University of California, Berkeley, NC 94720; USA;<email>crushworth@berkeley.edu</email></nlm:aff></affiliation></author><author><name sortKey="Baskar, R" sort="Baskar, R" uniqKey="Baskar R" first="R." last="Baskar">R. Baskar</name><affiliation><nlm:aff id="af5-genes-09-00185">Department of Biotechnology, Indian Institute of Technology. Sardar Patel road, 600036 Chennai, India;<email>rbaskar@iitm.ac.in</email></nlm:aff></affiliation></author><author><name sortKey="Smetanin, Dmitry" sort="Smetanin, Dmitry" uniqKey="Smetanin D" first="Dmitry" last="Smetanin">Dmitry Smetanin</name><affiliation><nlm:aff id="af6-genes-09-00185">Department of Plant and Microbial Biology Zurich-Basel Plant Science Center, University of Zurich, Zollikerstrasse 107, 8008 Zurich; Switzerland;<email>dmitry.smetanin@botinst.uzh.ch</email> (D.S.);<email>grossnik@botinst.uzh.ch</email> (U.G.)</nlm:aff></affiliation></author><author><name sortKey="Schmutz, Jeremy" sort="Schmutz, Jeremy" uniqKey="Schmutz J" first="Jeremy" last="Schmutz">Jeremy Schmutz</name><affiliation><nlm:aff id="af7-genes-09-00185">Department of Energy Joint Genome Institute, Walnut Creek, CA 94598; USA;<email>jschmutz@hudsonalpha.org</email> (J.S.);<email>dsrokhsar@gmail.com</email> (D.S.R.)</nlm:aff></affiliation><affiliation><nlm:aff id="af8-genes-09-00185">HudsonAlpha Institute of Biotechnology, Huntsville, AL 35806; USA</nlm:aff></affiliation></author><author><name sortKey="Rokhsar, Daniel S" sort="Rokhsar, Daniel S" uniqKey="Rokhsar D" first="Daniel S." last="Rokhsar">Daniel S. Rokhsar</name><affiliation><nlm:aff id="af7-genes-09-00185">Department of Energy Joint Genome Institute, Walnut Creek, CA 94598; USA;<email>jschmutz@hudsonalpha.org</email> (J.S.);<email>dsrokhsar@gmail.com</email> (D.S.R.)</nlm:aff></affiliation></author><author><name sortKey="Mitchell Olds, Thomas" sort="Mitchell Olds, Thomas" uniqKey="Mitchell Olds T" first="Thomas" last="Mitchell-Olds">Thomas Mitchell-Olds</name><affiliation><nlm:aff id="af9-genes-09-00185">Department of Biology, Duke University, Durham, NC 27708-0338; USA;<email>tmo1@duke.edu</email></nlm:aff></affiliation></author><author><name sortKey="Grossniklaus, Ueli" sort="Grossniklaus, Ueli" uniqKey="Grossniklaus U" first="Ueli" last="Grossniklaus">Ueli Grossniklaus</name><affiliation><nlm:aff id="af6-genes-09-00185">Department of Plant and Microbial Biology Zurich-Basel Plant Science Center, University of Zurich, Zollikerstrasse 107, 8008 Zurich; Switzerland;<email>dmitry.smetanin@botinst.uzh.ch</email> (D.S.);<email>grossnik@botinst.uzh.ch</email> (U.G.)</nlm:aff></affiliation></author><author><name sortKey="Brukhin, Vladimir" sort="Brukhin, Vladimir" uniqKey="Brukhin V" first="Vladimir" last="Brukhin">Vladimir Brukhin</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation><affiliation><nlm:aff id="af10-genes-09-00185">Department of Plant Embryology and Reproductive Biology, Komarov Botanical Institute RAS, 197376 St. Petersburg, Russia</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29597328</idno><idno type="pmc">5924527</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5924527</idno><idno type="RBID">PMC:5924527</idno><idno type="doi">10.3390/genes9040185</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000C93</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000C93</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Assembly of the <italic>Boechera retrofracta</italic> Genome and Evolutionary Analysis of Apomixis-Associated Genes</title><author><name sortKey="Kliver, Sergei" sort="Kliver, Sergei" uniqKey="Kliver S" first="Sergei" last="Kliver">Sergei Kliver</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation><affiliation><nlm:aff id="af2-genes-09-00185">All-Russia Research Institute for Agricultural Microbiology, Podbelskogo sh. 3, Pushkin, 196608 St. Petersburg, Russia</nlm:aff></affiliation></author><author><name sortKey="Rayko, Mike" sort="Rayko, Mike" uniqKey="Rayko M" first="Mike" last="Rayko">Mike Rayko</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Komissarov, Alexey" sort="Komissarov, Alexey" uniqKey="Komissarov A" first="Alexey" last="Komissarov">Alexey Komissarov</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Bakin, Evgeny" sort="Bakin, Evgeny" uniqKey="Bakin E" first="Evgeny" last="Bakin">Evgeny Bakin</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Zhernakova, Daria" sort="Zhernakova, Daria" uniqKey="Zhernakova D" first="Daria" last="Zhernakova">Daria Zhernakova</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation></author><author><name sortKey="Prasad, Kasavajhala" sort="Prasad, Kasavajhala" uniqKey="Prasad K" first="Kasavajhala" last="Prasad">Kasavajhala Prasad</name><affiliation><nlm:aff id="af3-genes-09-00185">Department of Biology, Colorado State University, Fort Collins, CO 80523; USA;<email>kasavajhalaprasad@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Rushworth, Catherine" sort="Rushworth, Catherine" uniqKey="Rushworth C" first="Catherine" last="Rushworth">Catherine Rushworth</name><affiliation><nlm:aff id="af4-genes-09-00185">University and Jepson Herbaria, University of California, Berkeley, NC 94720; USA;<email>crushworth@berkeley.edu</email></nlm:aff></affiliation></author><author><name sortKey="Baskar, R" sort="Baskar, R" uniqKey="Baskar R" first="R." last="Baskar">R. Baskar</name><affiliation><nlm:aff id="af5-genes-09-00185">Department of Biotechnology, Indian Institute of Technology. Sardar Patel road, 600036 Chennai, India;<email>rbaskar@iitm.ac.in</email></nlm:aff></affiliation></author><author><name sortKey="Smetanin, Dmitry" sort="Smetanin, Dmitry" uniqKey="Smetanin D" first="Dmitry" last="Smetanin">Dmitry Smetanin</name><affiliation><nlm:aff id="af6-genes-09-00185">Department of Plant and Microbial Biology Zurich-Basel Plant Science Center, University of Zurich, Zollikerstrasse 107, 8008 Zurich; Switzerland;<email>dmitry.smetanin@botinst.uzh.ch</email> (D.S.);<email>grossnik@botinst.uzh.ch</email> (U.G.)</nlm:aff></affiliation></author><author><name sortKey="Schmutz, Jeremy" sort="Schmutz, Jeremy" uniqKey="Schmutz J" first="Jeremy" last="Schmutz">Jeremy Schmutz</name><affiliation><nlm:aff id="af7-genes-09-00185">Department of Energy Joint Genome Institute, Walnut Creek, CA 94598; USA;<email>jschmutz@hudsonalpha.org</email> (J.S.);<email>dsrokhsar@gmail.com</email> (D.S.R.)</nlm:aff></affiliation><affiliation><nlm:aff id="af8-genes-09-00185">HudsonAlpha Institute of Biotechnology, Huntsville, AL 35806; USA</nlm:aff></affiliation></author><author><name sortKey="Rokhsar, Daniel S" sort="Rokhsar, Daniel S" uniqKey="Rokhsar D" first="Daniel S." last="Rokhsar">Daniel S. Rokhsar</name><affiliation><nlm:aff id="af7-genes-09-00185">Department of Energy Joint Genome Institute, Walnut Creek, CA 94598; USA;<email>jschmutz@hudsonalpha.org</email> (J.S.);<email>dsrokhsar@gmail.com</email> (D.S.R.)</nlm:aff></affiliation></author><author><name sortKey="Mitchell Olds, Thomas" sort="Mitchell Olds, Thomas" uniqKey="Mitchell Olds T" first="Thomas" last="Mitchell-Olds">Thomas Mitchell-Olds</name><affiliation><nlm:aff id="af9-genes-09-00185">Department of Biology, Duke University, Durham, NC 27708-0338; USA;<email>tmo1@duke.edu</email></nlm:aff></affiliation></author><author><name sortKey="Grossniklaus, Ueli" sort="Grossniklaus, Ueli" uniqKey="Grossniklaus U" first="Ueli" last="Grossniklaus">Ueli Grossniklaus</name><affiliation><nlm:aff id="af6-genes-09-00185">Department of Plant and Microbial Biology Zurich-Basel Plant Science Center, University of Zurich, Zollikerstrasse 107, 8008 Zurich; Switzerland;<email>dmitry.smetanin@botinst.uzh.ch</email> (D.S.);<email>grossnik@botinst.uzh.ch</email> (U.G.)</nlm:aff></affiliation></author><author><name sortKey="Brukhin, Vladimir" sort="Brukhin, Vladimir" uniqKey="Brukhin V" first="Vladimir" last="Brukhin">Vladimir Brukhin</name><affiliation><nlm:aff id="af1-genes-09-00185">Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</nlm:aff></affiliation><affiliation><nlm:aff id="af10-genes-09-00185">Department of Plant Embryology and Reproductive Biology, Komarov Botanical Institute RAS, 197376 St. Petersburg, Russia</nlm:aff></affiliation></author></analytic><series><title level="j">Genes</title><idno type="eISSN">2073-4425</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Closely related to the model plant <italic>Arabidopsis thaliana</italic>, the genus <italic>Boechera</italic> is known to contain both sexual and apomictic species or accessions. <italic>Boechera retrofracta</italic> is a diploid sexually reproducing species and is thought to be an ancestral parent species of apomictic species. Here we report the de novo assembly of the <italic>B. retrofracta</italic> genome using short Illumina and Roche reads from 1 paired-end and 3 mate pair libraries. The distribution of 23-mers from the paired end library has indicated a low level of heterozygosity and the presence of detectable duplications and triplications. The genome size was estimated to be equal 227 Mb. N50 of the assembled scaffolds was 2.3 Mb. Using a hybrid approach that combines homology-based and de novo methods 27,048 protein-coding genes were predicted. Also repeats, transfer RNA (tRNA) and ribosomal RNA (rRNA) genes were annotated. Finally, genes of <italic>B. retrofracta</italic> and 6 other Brassicaceae species were used for phylogenetic tree reconstruction. In addition, we explored the histidine exonuclease <italic>APOLLO</italic> locus, related to apomixis in <italic>Boechera</italic>, and proposed model of its evolution through the series of duplications. An assembled genome of <italic>B. retrofracta</italic> will help in the challenging assembly of the highly heterozygous genomes of hybrid apomictic species<italic>.</italic></p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Sharbel, T F" uniqKey="Sharbel T">T.F. Sharbel</name></author><author><name sortKey="Mitchell Olds, T" uniqKey="Mitchell Olds T">T. Mitchell-Olds</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Schranz, M E" uniqKey="Schranz M">M.E. Schranz</name></author><author><name sortKey="Dobes, C" uniqKey="Dobes C">C. Dobes</name></author><author><name sortKey="Koch, M A" uniqKey="Koch M">M.A. Koch</name></author><author><name sortKey="Mitchell Olds, T" uniqKey="Mitchell Olds T">T. Mitchell-Olds</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Naumova, T N" uniqKey="Naumova T">T.N. Naumova</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aliyu, O M" uniqKey="Aliyu O">O.M. Aliyu</name></author><author><name sortKey="Schranz, M E" uniqKey="Schranz M">M.E. Schranz</name></author><author><name sortKey="Sharbel, T F" uniqKey="Sharbel T">T.F. Sharbel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Koltunow, A M" uniqKey="Koltunow A">A.M. Koltunow</name></author><author><name sortKey="Grossniklaus, U" uniqKey="Grossniklaus U">U. Grossniklaus</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rodriguez Leal, D" uniqKey="Rodriguez Leal D">D. Rodríguez-Leal</name></author><author><name sortKey="Vielle Calzada, J P" uniqKey="Vielle Calzada J">J.P. Vielle-Calzada</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brukhin, V" uniqKey="Brukhin V">V. Brukhin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Windham, M D" uniqKey="Windham M">M.D. Windham</name></author><author><name sortKey="Al Shehbaz, I A" uniqKey="Al Shehbaz I">I.A. Al-Shehbaz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Windham, M D" uniqKey="Windham M">M.D. Windham</name></author><author><name sortKey="Al Shehbaz, I A" uniqKey="Al Shehbaz I">I.A. Al-Shehbaz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lovell, J T" uniqKey="Lovell J">J.T. Lovell</name></author><author><name sortKey="Williamson, R J" uniqKey="Williamson R">R.J. Williamson</name></author><author><name sortKey="Wright, S I" uniqKey="Wright S">S.I. Wright</name></author><author><name sortKey="Mckay, J K" uniqKey="Mckay J">J.K. McKay</name></author><author><name sortKey="Sharbel, T F" uniqKey="Sharbel T">T.F. Sharbel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rushworth, C A" uniqKey="Rushworth C">C.A. Rushworth</name></author><author><name sortKey="Song, B H" uniqKey="Song B">B.H. Song</name></author><author><name sortKey="Lee, C R" uniqKey="Lee C">C.R. Lee</name></author><author><name sortKey="Mitchell Olds, T" uniqKey="Mitchell Olds T">T. Mitchell-Olds</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Beck, J B" uniqKey="Beck J">J.B. Beck</name></author><author><name sortKey="Alexander, P J" uniqKey="Alexander P">P.J. Alexander</name></author><author><name sortKey="Allphin, L" uniqKey="Allphin L">L. Allphin</name></author><author><name sortKey="Al Shehbaz, I A" uniqKey="Al Shehbaz I">I.A. Al-Shehbaz</name></author><author><name sortKey="Rushworth, C" uniqKey="Rushworth C">C. Rushworth</name></author><author><name sortKey="Bailey, C D" uniqKey="Bailey C">C.D. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Genes (Basel)</journal-id><journal-id journal-id-type="iso-abbrev">Genes (Basel)</journal-id><journal-id journal-id-type="publisher-id">genes</journal-id><journal-title-group><journal-title>Genes</journal-title></journal-title-group><issn pub-type="epub">2073-4425</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29597328</article-id><article-id pub-id-type="pmc">5924527</article-id><article-id pub-id-type="doi">10.3390/genes9040185</article-id><article-id pub-id-type="publisher-id">genes-09-00185</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Assembly of the <italic>Boechera retrofracta</italic> Genome and Evolutionary Analysis of Apomixis-Associated Genes</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Kliver</surname><given-names>Sergei</given-names></name><xref ref-type="aff" rid="af1-genes-09-00185">1</xref><xref ref-type="aff" rid="af2-genes-09-00185">2</xref></contrib><contrib contrib-type="author"><name><surname>Rayko</surname><given-names>Mike</given-names></name><xref ref-type="aff" rid="af1-genes-09-00185">1</xref></contrib><contrib contrib-type="author"><name><surname>Komissarov</surname><given-names>Alexey</given-names></name><xref ref-type="aff" rid="af1-genes-09-00185">1</xref></contrib><contrib contrib-type="author"><name><surname>Bakin</surname><given-names>Evgeny</given-names></name><xref ref-type="aff" rid="af1-genes-09-00185">1</xref></contrib><contrib contrib-type="author"><name><surname>Zhernakova</surname><given-names>Daria</given-names></name><xref ref-type="aff" rid="af1-genes-09-00185">1</xref></contrib><contrib contrib-type="author"><name><surname>Prasad</surname><given-names>Kasavajhala</given-names></name><xref ref-type="aff" rid="af3-genes-09-00185">3</xref></contrib><contrib contrib-type="author"><name><surname>Rushworth</surname><given-names>Catherine</given-names></name><xref ref-type="aff" rid="af4-genes-09-00185">4</xref></contrib><contrib contrib-type="author"><name><surname>Baskar</surname><given-names>R.</given-names></name><xref ref-type="aff" rid="af5-genes-09-00185">5</xref></contrib><contrib contrib-type="author"><name><surname>Smetanin</surname><given-names>Dmitry</given-names></name><xref ref-type="aff" rid="af6-genes-09-00185">6</xref></contrib><contrib contrib-type="author"><name><surname>Schmutz</surname><given-names>Jeremy</given-names></name><xref ref-type="aff" rid="af7-genes-09-00185">7</xref><xref ref-type="aff" rid="af8-genes-09-00185">8</xref></contrib><contrib contrib-type="author"><name><surname>Rokhsar</surname><given-names>Daniel S.</given-names></name><xref ref-type="aff" rid="af7-genes-09-00185">7</xref></contrib><contrib contrib-type="author"><name><surname>Mitchell-Olds</surname><given-names>Thomas</given-names></name><xref ref-type="aff" rid="af9-genes-09-00185">9</xref></contrib><contrib contrib-type="author"><name><surname>Grossniklaus</surname><given-names>Ueli</given-names></name><xref ref-type="aff" rid="af6-genes-09-00185">6</xref></contrib><contrib contrib-type="author"><name><surname>Brukhin</surname><given-names>Vladimir</given-names></name><xref ref-type="aff" rid="af1-genes-09-00185">1</xref><xref ref-type="aff" rid="af10-genes-09-00185">10</xref><xref rid="c1-genes-09-00185" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-genes-09-00185"><label>1</label>Dobzhansky Center for Genome Bioinformatics, St. Petersburg State Universit, Sredniy Prospekt, 41, Vasilievsky Island, 199004 St. Petersburg, Russia;<email>mahajrod@gmail.com</email> (S.K.);<email>mikerayko@gmail.com</email> (M.R.);<email>ad3002@gmail.com</email> (A.K.);<email>eugene.bakin@gmail.com</email> (E.B.);<email>dashzhernakova@gmail.com</email> (D.Z.)</aff><aff id="af2-genes-09-00185"><label>2</label>All-Russia Research Institute for Agricultural Microbiology, Podbelskogo sh. 3, Pushkin, 196608 St. Petersburg, Russia</aff><aff id="af3-genes-09-00185"><label>3</label>Department of Biology, Colorado State University, Fort Collins, CO 80523; USA;<email>kasavajhalaprasad@gmail.com</email></aff><aff id="af4-genes-09-00185"><label>4</label>University and Jepson Herbaria, University of California, Berkeley, NC 94720; USA;<email>crushworth@berkeley.edu</email></aff><aff id="af5-genes-09-00185"><label>5</label>Department of Biotechnology, Indian Institute of Technology. Sardar Patel road, 600036 Chennai, India;<email>rbaskar@iitm.ac.in</email></aff><aff id="af6-genes-09-00185"><label>6</label>Department of Plant and Microbial Biology Zurich-Basel Plant Science Center, University of Zurich, Zollikerstrasse 107, 8008 Zurich; Switzerland;<email>dmitry.smetanin@botinst.uzh.ch</email> (D.S.);<email>grossnik@botinst.uzh.ch</email> (U.G.)</aff><aff id="af7-genes-09-00185"><label>7</label>Department of Energy Joint Genome Institute, Walnut Creek, CA 94598; USA;<email>jschmutz@hudsonalpha.org</email> (J.S.);<email>dsrokhsar@gmail.com</email> (D.S.R.)</aff><aff id="af8-genes-09-00185"><label>8</label>HudsonAlpha Institute of Biotechnology, Huntsville, AL 35806; USA</aff><aff id="af9-genes-09-00185"><label>9</label>Department of Biology, Duke University, Durham, NC 27708-0338; USA;<email>tmo1@duke.edu</email></aff><aff id="af10-genes-09-00185"><label>10</label>Department of Plant Embryology and Reproductive Biology, Komarov Botanical Institute RAS, 197376 St. Petersburg, Russia</aff><author-notes><corresp id="c1-genes-09-00185"><label>*</label>Correspondence: <email>vbrukhin@gmail.com</email>; Tel.: +7-965-046-5605</corresp></author-notes><pub-date pub-type="epub"><day>28</day><month>3</month><year>2018</year></pub-date><pub-date pub-type="collection"><month>4</month><year>2018</year></pub-date><volume>9</volume><issue>4</issue><elocation-id>185</elocation-id><history><date date-type="received"><day>14</day><month>2</month><year>2018</year></date><date date-type="accepted"><day>22</day><month>3</month><year>2018</year></date></history><permissions><copyright-statement>© 2018 by the authors.</copyright-statement><copyright-year>2018</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>Closely related to the model plant <italic>Arabidopsis thaliana</italic>, the genus <italic>Boechera</italic> is known to contain both sexual and apomictic species or accessions. <italic>Boechera retrofracta</italic> is a diploid sexually reproducing species and is thought to be an ancestral parent species of apomictic species. Here we report the de novo assembly of the <italic>B. retrofracta</italic> genome using short Illumina and Roche reads from 1 paired-end and 3 mate pair libraries. The distribution of 23-mers from the paired end library has indicated a low level of heterozygosity and the presence of detectable duplications and triplications. The genome size was estimated to be equal 227 Mb. N50 of the assembled scaffolds was 2.3 Mb. Using a hybrid approach that combines homology-based and de novo methods 27,048 protein-coding genes were predicted. Also repeats, transfer RNA (tRNA) and ribosomal RNA (rRNA) genes were annotated. Finally, genes of <italic>B. retrofracta</italic> and 6 other Brassicaceae species were used for phylogenetic tree reconstruction. In addition, we explored the histidine exonuclease <italic>APOLLO</italic> locus, related to apomixis in <italic>Boechera</italic>, and proposed model of its evolution through the series of duplications. An assembled genome of <italic>B. retrofracta</italic> will help in the challenging assembly of the highly heterozygous genomes of hybrid apomictic species<italic>.</italic></p></abstract><kwd-group><kwd><italic>Boechera</italic></kwd><kwd>Brassicaceae</kwd><kwd>genome</kwd><kwd>assembly</kwd><kwd>annotation</kwd><kwd>apomixis</kwd></kwd-group></article-meta></front><body><sec id="sec1-genes-09-00185"><title>1. Introduction</title><p>Among over the 370 genera belonging to the family Brassicaceae (Cruciferae), only the genus <italic>Boechera</italic> shows asexual reproduction by seeds [<xref rid="B1-genes-09-00185" ref-type="bibr">1</xref>,<xref rid="B2-genes-09-00185" ref-type="bibr">2</xref>,<xref rid="B3-genes-09-00185" ref-type="bibr">3</xref>,<xref rid="B4-genes-09-00185" ref-type="bibr">4</xref>]. Apomixis is defined as asexual reproduction through seeds that results in progeny identical to the maternal plant. The harnessing of apomixis is widely considered as a key enabling technology for crop improvement because it allows the fixation of any heterozygous genotype, leading to simpler and faster breeding schemes [<xref rid="B5-genes-09-00185" ref-type="bibr">5</xref>,<xref rid="B6-genes-09-00185" ref-type="bibr">6</xref>,<xref rid="B7-genes-09-00185" ref-type="bibr">7</xref>]. The <italic>Boechera</italic> genus includes 110 sexual and apomictic species, widely distributed in North America. Plants from the <italic>Boechera</italic> genus are represented by biannual and perennial herbs with a chromosome base number of <italic>n</italic> = 7 [<xref rid="B8-genes-09-00185" ref-type="bibr">8</xref>,<xref rid="B9-genes-09-00185" ref-type="bibr">9</xref>].</p><p>Apomixis in the <italic>Boechera</italic> genus is of special interest because it can occur at the diploid level, which is very rare [<xref rid="B1-genes-09-00185" ref-type="bibr">1</xref>,<xref rid="B2-genes-09-00185" ref-type="bibr">2</xref>,<xref rid="B3-genes-09-00185" ref-type="bibr">3</xref>,<xref rid="B4-genes-09-00185" ref-type="bibr">4</xref>,<xref rid="B5-genes-09-00185" ref-type="bibr">5</xref>,<xref rid="B6-genes-09-00185" ref-type="bibr">6</xref>,<xref rid="B7-genes-09-00185" ref-type="bibr">7</xref>,<xref rid="B8-genes-09-00185" ref-type="bibr">8</xref>]. Furthermore, the phylogenetic proximity of <italic>Boechera</italic> to the model plant <italic>Arabidopsis thaliana</italic> is attractive for potential functional studies. Although the genus <italic>Boechera</italic> includes both sexual and apomictic species and accessions that are of variable ploidy and geographical origin, search for homologous sequences are feasible across the genus [<xref rid="B10-genes-09-00185" ref-type="bibr">10</xref>]. The sexual accessions of <italic>Boechera</italic> are self-compatible and largely self-pollinating [<xref rid="B11-genes-09-00185" ref-type="bibr">11</xref>], unlike the sexual ancestors of most other apomicts, which are typically self-incompatible and cross-pollinating [<xref rid="B12-genes-09-00185" ref-type="bibr">12</xref>]. This inbreeding causes low heterozygosity in sexual <italic>Boechera</italic> species. Apomictic <italic>Boechera</italic> accessions have likely arisen through independent hybridization events [<xref rid="B13-genes-09-00185" ref-type="bibr">13</xref>]. Their hybridogenic origin is supported by the aberrant structure of their chromosomes, as they are often observed as a consequence of hybridization, leading to alloploidy, aneuploidy, the replacement of homeologous chromosomes, and aberrant chromosomes [<xref rid="B13-genes-09-00185" ref-type="bibr">13</xref>,<xref rid="B14-genes-09-00185" ref-type="bibr">14</xref>].</p><p>Certain apomictic <italic>Boechera</italic> accessions are hypothesized to have arisen through hybridization between sexual <italic>Boechera stricta</italic> and <italic>Boechera retrofracta</italic> (<xref ref-type="fig" rid="genes-09-00185-f001">Figure 1</xref>). <italic>Boechera retrofracta</italic> was previously included within <italic>Boechera holboellii</italic> (sensu lato) [<xref rid="B15-genes-09-00185" ref-type="bibr">15</xref>]. Up to now only the genome sequence of <italic>B. stricta</italic> was available [<xref rid="B16-genes-09-00185" ref-type="bibr">16</xref>], while the genome of <italic>B. retrofracta</italic> has not been assembled yet.</p><p>In this paper, we present the assembly and annotation of the <italic>B. retrofracta</italic> genome. The availability of the <italic>B. retrofracta</italic> genome sequence together with the previously assembled <italic>B. stricta</italic> genome will greatly help in the assembly and annotation of related apomictic hybrid species and provide the basis to investigate the peculiarities of hybridization events, chromosomal organization, the stability of apomictic genomes, and the genetic factors underlying apomixis. The performed assembly and annotation allowed us to analyze of the <italic>APOLLO</italic> (APOmixis-Linked LOcus) genes, that are associated with apomixis in <italic>Boechera</italic>.</p></sec><sec id="sec2-genes-09-00185"><title>2. Materials and Methods </title><sec id="sec2dot1-genes-09-00185"><title>2.1. Sample Information </title><p>The reference <italic>B. retrofracta</italic> genotype was collected in Panther Creek, Lemhi County, Idaho, at 45°18′11.9″ N 114°22′35.9″ W, 1610 m elevation (<xref ref-type="fig" rid="genes-09-00185-f001">Figure 1</xref>). Plant growth, DNA extraction, and library construction were the same as with <italic>B. stricta</italic> [<xref rid="B16-genes-09-00185" ref-type="bibr">16</xref>]. Briefly, seedlings were germinated in aseptic culture in half-strength Murashige and Skoog (MS) liquid medium. Cell nuclei were used for isolation of clean high-molecular-size nuclear DNA in Tris-EDTA (TE) buffer. </p></sec><sec id="sec2dot2-genes-09-00185"><title>2.2. Sequencing Strategy</title><p>The <italic>B. retrofracta</italic> genome was sequenced within the JGI Community Sequencing Project to produce sequence data for the <italic>Boechera</italic> genus [<xref rid="B17-genes-09-00185" ref-type="bibr">17</xref>]. Six libraries were constructed and sequenced using three platforms including Illumina, Roche, and Sanger: one paired-end (PE) library, four mate pairs (MP) libraries and one Sanger bacterial artificial chromosome (BAC) end library. Read length and actual insert sizes for each library are given in <xref ref-type="app" rid="app1-genes-09-00185">Appendix A</xref> (<xref ref-type="table" rid="genes-09-00185-t0A1">Table A1</xref>). This sequencing scheme was specially developed for the initial contig assembly by the DISCOVAR assembler [<xref rid="B18-genes-09-00185" ref-type="bibr">18</xref>], followed by scaffolding. Construction of genomic libraries and sequencing were performed following Lee et al [<xref rid="B16-genes-09-00185" ref-type="bibr">16</xref>].</p></sec><sec id="sec2dot3-genes-09-00185"><title>2.3. Raw Data Filtration and Pre-Processing</title><p>Filtration of the PE library LIB400 was performed in two stages. First, reads containing long adapter fragments were removed using Cookiecutter [<xref rid="B19-genes-09-00185" ref-type="bibr">19</xref>]. Then Trimmomatic [<xref rid="B20-genes-09-00185" ref-type="bibr">20</xref>] was used to filter out reads with short adapter fragments. However, according to the DISCOVAR requirements no trimming or quality filtration was performed at those two stages. Only whole reads contaminated by adapters were discarded.</p><p>To process Illumina MP libraries LIB5000 and LIB7000 the NextClip [<xref rid="B21-genes-09-00185" ref-type="bibr">21</xref>] tool was modified to handle Cre-Lox libraries. It is important to note that original NextClip uses a very simple algorithm to align linker sequences to reads. It takes into account only the number of matching bases. As the CreLox linker is significantly longer than the Nextera linker, the number of false hits may significantly increase. To mitigate this effect, a requirement for the presence of a continuous 9-bp core alignment was added. The modified tool was named CreClip and can be found in [<xref rid="B22-genes-09-00185" ref-type="bibr">22</xref>].</p><p>Reads from Roche MP Libraries LIB4000R and LIB24000R were split into “forward” and “reverse” segments separated by linker. Then, low quality ends were trimmed from “reverse” segments by Trimmomatic. Finally, reverse segments were reverse complemented to mimic to Illumina MP libraries.</p></sec><sec id="sec2dot4-genes-09-00185"><title>2.4. Genome Size Estimation</title><p>Estimation of the genome size based on the 23-mer distribution (as well as other <italic>k</italic>-mer based statistics) was performed using the KrATER software [<xref rid="B23-genes-09-00185" ref-type="bibr">23</xref>] on the LIB400 library and further compared with the previous estimations of <italic>Boechera</italic> genus [<xref rid="B24-genes-09-00185" ref-type="bibr">24</xref>].</p></sec><sec id="sec2dot5-genes-09-00185"><title>2.5. Genome Assembly and Quality Evaluation</title><p>At the assembly stage initial contigs were constructed from the filtered LIB400 reads by DISCOVAR. Then, the obtained contigs were extended using a BAC end sequencing (BES) library and the SSPACE scaffolder [<xref rid="B25-genes-09-00185" ref-type="bibr">25</xref>].</p><p>Before scaffolding the assessment of the actual (mean) insert size was performed. Filtered reads from all libraries were aligned to initial contigs by Burrows–Wheeler Aligner (BWA) [<xref rid="B26-genes-09-00185" ref-type="bibr">26</xref>]. For each library, only alignments to contigs with 3× length of the target insert size were used in the estimation (<xref ref-type="table" rid="genes-09-00185-t001">Table 1</xref>) to minimize alignment artifacts. Next, the extended contigs were scaffolded by SSPACE in two stages: at the first stage, all four MP libraries (LIB4000R, LIB5000, LIB7000, LIB24000R) were used to produce raw scaffolds, at the second stage, raw scaffolds were linked to the intermediate scaffolds using the BES library only. Scaffolding was carried out in several stages because different options were required to utilize the BES data. Gap closing in the intermediate scaffolds was performed using GapCloser (a module for SOAPdenovo2) [<xref rid="B27-genes-09-00185" ref-type="bibr">27</xref>] on the LIB400 library only. Finally, all scaffolds with a length of less than 250 bp (i.e., less than read length of LIB400, the library used for initial contig construction) were filtered out, as the corresponding short fragments most likely are the assembly artifacts. Integrity of the assembly was verified by Core Eukaryotic Genes Mapping Approach (CEGMA) [<xref rid="B28-genes-09-00185" ref-type="bibr">28</xref>] and Benchmarking Universal Single-Copy Orthologs (BUSCO) [<xref rid="B29-genes-09-00185" ref-type="bibr">29</xref>]. A schematic diagram of the assembly pipeline is shown in <xref ref-type="fig" rid="genes-09-00185-f0A1">Figure A1</xref> in <xref ref-type="app" rid="app1-genes-09-00185">Appendix A</xref>.</p></sec><sec id="sec2dot6-genes-09-00185"><title>2.6. Repeats Analysis</title><p>A de novo repeat identification in the <italic>B. retrofracta</italic> genome was performed using RepeatModeler [<xref rid="B30-genes-09-00185" ref-type="bibr">30</xref>] with default parameters. The obtained repeat library was combined with <italic>Arabidopsis thaliana</italic> repeats from RepBase [<xref rid="B31-genes-09-00185" ref-type="bibr">31</xref>], and the merged library was used to annotate repeats by RepeatMasker [<xref rid="B32-genes-09-00185" ref-type="bibr">32</xref>]. Then repeats in the <italic>B. retrofracta</italic> genome were softmasked by Bedtools [<xref rid="B33-genes-09-00185" ref-type="bibr">33</xref>] for the prediction of protein coding genes. Also, masking of tandem and interspersed repeats by tandem repeats finder (TRF) [<xref rid="B34-genes-09-00185" ref-type="bibr">34</xref>] and WindowMasker [<xref rid="B35-genes-09-00185" ref-type="bibr">35</xref>], respectively, were performed.</p></sec><sec id="sec2dot7-genes-09-00185"><title>2.7. Variants Calling and Genotyping</title><p>For variant calling and genotyping filtered reads were aligned to the assembled genome using BWA mem with default options. Next, the Genome Analysis Toolkit (GATK) pipeline [<xref rid="B36-genes-09-00185" ref-type="bibr">36</xref>] for variant calling was applied in the following way: duplicates were marked using Picard MarkDuplicates (Broad Institute, Cambridge, MA, USA), realigned reads at indels, and, finally, HaplotypeCaller (Broad Institute) was used to call variants. Only single nucleotide polymorphisms (SNPs) and indels were kept passing the following filtering criteria: QualByDepth (QD) > 2.0, FisherStrand (FS) < 20.0, RMSMappingQuality (MQ) > 40.0, MappingQualityRankSumTest (MQRankSum) > −12.5, ReadPosRankSumTest (ReadPosRankSum) > −8.0 for SNPs, and QualByDepth (QD) > 2.0, FisherStrand (FS) < 20.0, ReadPosRankSumTest (ReadPosRankSum) > −20.0 for indels, respectively. Finally, the variants falling into the repeats masked by RepeatMasker were excluded.</p></sec><sec id="sec2dot8-genes-09-00185"><title>2.8. Prediction of Protein-Coding Genes and Non-Coding RNA</title><p>The prediction of protein-coding genes was performed using a combined approach that synthesizes both homology-based and de novo predictions, where de novo predictions are used only to fill gaps and to extend the homology-based predictions. Pure de novo predictions were filtered out.</p><p>As homology-based evidence for gene presence, we have used proteins and transcripts of five closely-related species. Proteins of the four reference species—<italic>Arabidopsis thaliana</italic> (assembly TAIR10), <italic>Brassica rapa</italic> (Brapa_1.0), <italic>Capsella rubella</italic> (Caprub1_0), and <italic>Eutrema salsugineum</italic> (Eutsalg1_0)—were aligned to the <italic>B. retrofracta</italic> assembly by Exonerate [<xref rid="B37-genes-09-00185" ref-type="bibr">37</xref>], using the Protein2Genome model with a maximum of three hits per protein. The obtained alignments were classified into the top (primary) and secondary hits; the coding sequence (CDS) fragments were cut from each side by 3 bp for the top hits and by 9 bp for the secondary hits. Transcripts of <italic>B. stricta</italic> (assembly v1.2, [<xref rid="B16-genes-09-00185" ref-type="bibr">16</xref>]) with marked CDS regions were also aligned to the <italic>B. retrofracta</italic> genome by Exonerate using the cDNA2Genome model leaving the other options unchanged. Alignments of CDS segments were not cut for top hits, but cut by 3 bp for secondary hits. </p><p>These truncated fragments were clustered and supplied as hints to the AUGUSTUS software package [<xref rid="B38-genes-09-00185" ref-type="bibr">38</xref>], and the CDS segments of genes were predicted in the soft-masked <italic>B. retrofracta</italic> assembly using <italic>A. thaliana</italic> gene models. Proteins were translated from the predicted genes and aligned by HMMER 3.1 [<xref rid="B39-genes-09-00185" ref-type="bibr">39</xref>] and BLAST [<xref rid="B40-genes-09-00185" ref-type="bibr">40</xref>] to the Pfam [<xref rid="B41-genes-09-00185" ref-type="bibr">41</xref>] and Swiss-Prot [<xref rid="B42-genes-09-00185" ref-type="bibr">42</xref>] databases, respectively. Only genes supported by the both hints and hits to one of the protein databases were retained; the rest were discarded. Transfer RNA (tRNA) and ribosomal RNA (rRNA) genes were predicted by tRNAscan-SE v1.3.1 [<xref rid="B43-genes-09-00185" ref-type="bibr">43</xref>] and Barrnap v0.6 [<xref rid="B44-genes-09-00185" ref-type="bibr">44</xref>], respectively.</p></sec><sec id="sec2dot9-genes-09-00185"><title>2.9. Phylogenetic Analysis</title><p>The longest proteins corresponding to each predicted gene of <italic>B. retrofracta</italic> and six other Brassicaceae species—<italic>B. stricta</italic> (assembly v1.2), <italic>A. thaliana</italic> (TAIR10), <italic>Arabidopsis lyrata</italic> (v.1.0)<italic>, Capsella rubella (Caprub1_0), Cardamine hirsuta</italic> (v1.0), and <italic>Eutrema salsugineum</italic> (Eutsalg1_0)—were aligned to profile Hidden Markov Models (HMM) of the braNOG subset from the eggNOG database [<xref rid="B45-genes-09-00185" ref-type="bibr">45</xref>] using HMMER. The top hits from the alignments were extracted and used for assignment of the corresponding proteins to orthologous groups, followed by extraction of single-copy orthologs.</p><p>To verify topology concordance and get a basis for future studies of positive selection, a species tree reconstruction was performed. Single-copy orthologous proteins of the seven species included in the analysis were aligned by multiple alignment using fast Fourier transform (MAFFT) [<xref rid="B46-genes-09-00185" ref-type="bibr">46</xref>]. Based on the obtained protein alignments, a maximum likelihood tree was reconstructed by RAxML v8.2 [<xref rid="B47-genes-09-00185" ref-type="bibr">47</xref>] with the PROTGAMMAAUTO option, and the JTT fitting model was tested with 1000 bootstrap replications. The tree was rooted with <italic>E. salsugineum</italic> as an outgroup. The resulting tree was drawn with FigTree software [<xref rid="B48-genes-09-00185" ref-type="bibr">48</xref>].</p></sec><sec id="sec2dot10-genes-09-00185"><title>2.10. APOLLO Evolution Analysis</title><p>The evolutionary history of <italic>APOLLO</italic> gene was inferred by using the Maximum Likelihood method. Initial alignment of corresponding CDS was performed using prank v.140110 [<xref rid="B49-genes-09-00185" ref-type="bibr">49</xref>] in codon-aware mode. The alignment result was further used for building phylogenetic tree basing on the Tamura-Nei model [<xref rid="B50-genes-09-00185" ref-type="bibr">50</xref>,<xref rid="B51-genes-09-00185" ref-type="bibr">51</xref>]. The tree with the highest log likelihood (−12,153.79) was selected (see <xref ref-type="sec" rid="sec3dot7-genes-09-00185">Section 3.7</xref>, <xref ref-type="fig" rid="genes-09-00185-f004">Figure 4</xref>). Initial tree(s) for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using the maximum composite likelihood (MCL) approach, and then selecting the topology with superior log likelihood value. All positions containing gaps and missing data were eliminated. There were a total of 1158 positions in the final dataset. Evolutionary analyses were conducted in MEGA7 [<xref rid="B52-genes-09-00185" ref-type="bibr">52</xref>].</p></sec><sec id="sec2dot11-genes-09-00185"><title>2.11. Whole-Genome Comparison</title><p>As a preliminary step for the future whole-genome comparison of different <italic>Boechera</italic> species a whole genome alignment was performed via Cactus multiple genome aligner [<xref rid="B53-genes-09-00185" ref-type="bibr">53</xref>] and further visualized with web-tool ClicO FS [<xref rid="B54-genes-09-00185" ref-type="bibr">54</xref>] based on Circos [<xref rid="B55-genes-09-00185" ref-type="bibr">55</xref>].</p><p>For further information about the initial data and results, see <xref ref-type="app" rid="app2-genes-09-00185">Appendix B</xref>.</p></sec></sec><sec id="sec3-genes-09-00185"><title>3. Results</title><sec id="sec3dot1-genes-09-00185"><title>3.1. k-mer Based Statistics </title><p><italic>k</italic>-mer spectrum built by KrATER [<xref rid="B23-genes-09-00185" ref-type="bibr">23</xref>] is shown in <xref ref-type="fig" rid="genes-09-00185-f002">Figure 2</xref>. The 23-mer distribution has a peak of erroneous 23-mers at 1× coverage corresponding to sequencing errors and one major peak at 371× coverage corresponding to diploid 23-mers (shared between homologous chromosomes), but no significant peak related to heterozygous genome positions was detected (<xref ref-type="fig" rid="genes-09-00185-f002">Figure 2</xref>). However, we detected several small additional peaks at double (737×) and triple (1120×) depth, which are probably related to duplications and triplications, respectively.</p><p>The genome size of <italic>B. retrofracta</italic> was estimated to be close to 227 Mbp, which is close to the previous estimations of a minimal genome size of 200 Mbp in the <italic>Boechera</italic> genus [<xref rid="B24-genes-09-00185" ref-type="bibr">24</xref>].</p></sec><sec id="sec3dot2-genes-09-00185"><title>3.2. Genome Assembly and Evaluation </title><p>We have achieved N50 of 2,297,899 bp, L50 of 25, and a total assembly length of 222.25 Mbp for the final scaffolds, which is very close to our 23-mer based estimation. Detailed statistics including N50 and total assembly values for every stage of the assembly pipeline are listed in <xref ref-type="table" rid="genes-09-00185-t001">Table 1</xref> and <xref ref-type="table" rid="genes-09-00185-t002">Table 2</xref>. It is important to note that the final assembly (<xref ref-type="table" rid="genes-09-00185-t001">Table 1</xref>, column final scaffolds) has smaller size than previous intermediate assemblies due to the last filtration step. All scaffolds shorter than 250 bp (a read length of LIB400) were treated as artifacts of assembly and were removed. However, size of final assembly (222.25 Mbp) is closer to estimated genome size (226.87 Mbp) than the size of intermediate assemblies.</p><p>Evaluation of the assembly completeness was performed using CEGMA [<xref rid="B28-genes-09-00185" ref-type="bibr">28</xref>] and BUSCO [<xref rid="B29-genes-09-00185" ref-type="bibr">29</xref>]. In the assembled genome 242 (97.58%) complete core eukaryotic genes (CEGs) were identified. Out of 1440 BUSCO genes from the Embryophyta, set only 12 (0.8%) genes were not found, 6 were fragmented, 36 (2.5%) were duplicated and 1422 (98.8%) were complete. This high fraction of complete BUSCO genes suggests high completeness of the assembly and its integrity at least in gene-coding regions.</p></sec><sec id="sec3dot3-genes-09-00185"><title>3.3. Repeats Annotation</title><p>In total approximately 85 Mbp (38.13%) of the assembly were masked. The detailed description of the annotated repeat types is listed in <xref ref-type="table" rid="genes-09-00185-t003">Table 3</xref>. It is important to note that a large number (10.96% of the assembly size) of interspersed repeats was not classified. The results are shown in <xref ref-type="table" rid="genes-09-00185-t004">Table 4</xref>.</p></sec><sec id="sec3dot4-genes-09-00185"><title>3.4. Variant Calling and Genotyping</title><p>In the genome 3341 SNPs and 1317 indels were detected. Among these, 103 (3.08%) SNPs and 97 (7.37%) indels were homozygous and, therefore, most likely artifacts of alignment or assembly or SNP calling. Mean heterozygous SNP and indel densities in non-masked regions (138 Mbp in total) are 0.0235 SNP and 0.0089 indel per Kbp, respectively, suggesting a very low heterozygosity of the <italic>B. retrofracta</italic> genome.</p></sec><sec id="sec3dot5-genes-09-00185"><title>3.5. Prediction of Protein-Coding Genes and Non-Coding RNAs </title><p>In total 27,048 genes with 28,269 transcripts were predicted. tRNA and rRNA genes predicted by tRNAscan-SE and Barrnap are given in <xref ref-type="table" rid="genes-09-00185-t005">Table 5</xref> and <xref ref-type="table" rid="genes-09-00185-t006">Table 6</xref> respectively. </p></sec><sec id="sec3dot6-genes-09-00185"><title>3.6. Species Tree Reconstruction</title><p>In course of the assignment of proteins to orthologous groups 8959 single-copy orthologs were identified among the seven species (<italic>B. retrofracta</italic>, <italic>B. stricta</italic>, <italic>A. thaliana</italic>, <italic>A. lyrata</italic>, <italic>C. rubella, C. hirsuta</italic>, and <italic>E. salsugineum</italic>). </p><p>The corresponding phylogenetic tree was rooted with <italic>E. salsugineum</italic> as an outgroup (<xref ref-type="fig" rid="genes-09-00185-f003">Figure 3</xref>). All nodes have a high support and no topology discordance was found with the tree reconstructed previously by Huang et al [<xref rid="B52-genes-09-00185" ref-type="bibr">52</xref>].</p></sec><sec id="sec3dot7-genes-09-00185"><title>3.7. Analysis of Evolution of the APOLLO Locus</title><p>Results from Corral et al. [<xref rid="B56-genes-09-00185" ref-type="bibr">56</xref>] suggest that <italic>APOLLO</italic> (aspartate glutamate aspartate aspartate histidine exonuclease) is one of the important apomixis-related genes in <italic>Boechera</italic>. It was shown that the <italic>APOLLO</italic> locus has several alleles with apomixis-associated polymorphisms. All studied apomictic plants carry at least one of the “apoalleles”, while both copies in sexual genotypes were “sexalleles”.</p><p>In this study we decided to take a closer look to this locus in our assembly and other Brassicaceae species in this study. Along with an exact copy of the <italic>APOLLO</italic> locus, we also found two other, more distant copies, which may indicate past duplication events. We searched for these orthologs in other species, and reconstructed phylogenetic tree (<xref ref-type="fig" rid="genes-09-00185-f004">Figure 4</xref>). All Brassicaceae genomes in the study also carried these three copies, related to the clusters of orthologous genes ENOG410BURN (<italic>APOLLO</italic> locus), ENOG410BUTR, and ENOG410C333 in the EggNOG database.</p><p>We observed that branches in the tree were grouped by genes rather than by species, suggesting that the triplication event took place before the separation of the Brassicaceae species in this study. It is worth noting that in <italic>Populus trichocarpa</italic> genome there is only one copy of these locus, which gives an upper-bound time estimate of the series of duplication events. </p><p>We also examined <italic>APOLLO</italic> alleles (both apo- and sex-alleles) described in <italic>Boechera ssp</italic>. by Corral et al. [<xref rid="B56-genes-09-00185" ref-type="bibr">56</xref>]. We can see that these alleles arise after the separation of the <italic>Boechera</italic> genus, and compose two separate clades. Given the fact that <italic>B.retrofracta</italic> and <italic>B.stricta</italic> are the sexual species, it was not surprising that in both cases all corresponding polymorphic sites were in the “sexallele”-state, and clustered with sex-alleles.</p><p>We calculated the Ka/Ks ratio for the internal branches in this tree and found that branch leading to apo-alleles is under positive selection (Ka/Ks 1.4646, the branch is shown in red in <xref ref-type="fig" rid="genes-09-00185-f004">Figure 4</xref>), which is typical for paralogues that are required to serve a novel function. </p><p>The <italic>APOLLO</italic> gene was initially described in <italic>A. thaliana</italic> as an exonuclease, protein NEN3, Q9CA74 in Uniprot database [<xref rid="B42-genes-09-00185" ref-type="bibr">42</xref>], probably involved in enucleation of sieve elements, whereas two other copies were described as NEN1 (Q9FLR0) and NEN2 (Q0V842). Given that, we may suggest an evolutionary scenario where, after the series of duplications, one of the NEN protein copies in the common ancestor of <italic>Boechera</italic> spp. might have acquired alter regulation, and might induce development of the apomictic reproduction from the ancestral “sexual” state, following by separation of the apomictic lineages.</p><p>That could explain the phenomena of the diploid apomictic <italic>Boechera</italic>, emerged as a result of duplication events rather than polyploidy.</p></sec><sec id="sec3dot8-genes-09-00185"><title>3.8. Whole-Genome Comparison</title><p>As an example of whole-genome comparison a Circos plot was built for <italic>B. retrofracta</italic> and <italic>B. stricta</italic> (<xref ref-type="app" rid="app3-genes-09-00185">Appendix C</xref>). Since both assemblies are performed on a scaffold level, it is difficult to highlight any large genome rearrangements. However, this plot is a visual way to represent the scatteredness of both assemblies.</p></sec></sec><sec id="sec4-genes-09-00185"><title>4. Discussion</title><p>In this study we present a de novo assembly and annotation of the genome of <italic>Boechera retrofracta</italic>, a perennial flowering plant belonging to Brassicaceae family that is native to North America. The genome of <italic>B. retrofracta</italic> demonstrated a very low level of heterozygosity compare to the genomes of apomictic accessions [<xref rid="B2-genes-09-00185" ref-type="bibr">2</xref>,<xref rid="B8-genes-09-00185" ref-type="bibr">8</xref>,<xref rid="B9-genes-09-00185" ref-type="bibr">9</xref>,<xref rid="B10-genes-09-00185" ref-type="bibr">10</xref>,<xref rid="B11-genes-09-00185" ref-type="bibr">11</xref>,<xref rid="B12-genes-09-00185" ref-type="bibr">12</xref>,<xref rid="B13-genes-09-00185" ref-type="bibr">13</xref>,<xref rid="B14-genes-09-00185" ref-type="bibr">14</xref>,<xref rid="B15-genes-09-00185" ref-type="bibr">15</xref>,<xref rid="B16-genes-09-00185" ref-type="bibr">16</xref>]. Notably, repeats in the genome of <italic>B. retrofracta</italic> occupied almost 40% of the genome space. Nearly half of them were long terminal repeats (LTRs) (18.27%). The genome size was found to be 227 Mb, nearly two-fold larger than the <italic>Arabidopsis thaliana</italic> genome (<xref ref-type="table" rid="genes-09-00185-t007">Table 7</xref>). At the same time the amount of protein-coding genes in the genome of <italic>B. retrofracta</italic> is slightly less then in the <italic>B. stricta</italic> and <italic>A. thaliana</italic> genomes and much less than that in the <italic>A. lyrata</italic> genome (<xref ref-type="table" rid="genes-09-00185-t001">Table 1</xref>). Despite the largest genome size, the number of predicted transcripts in <italic>B. retrofracta</italic> is the smallest among the four Brassicaceae species compared (<xref ref-type="table" rid="genes-09-00185-t001">Table 1</xref>). The presence of a slightly greater number of genes in <italic>B. stricta</italic> compared with <italic>B. retrofracta</italic>, despite a smaller genome size, may be associated with aneuploidy of the chromosomal fragments, or genome rearrangements occurred as a result of interhybridization, which is characteristic of many <italic>Boechera</italic> species and accessions.</p><p>As an example of how the genome of the sexual species <italic>B. retrofracta</italic> could be used to study evolution and origin of apomixis, we performed an evolutionary analysis of the three alleles of the <italic>APOLLO</italic> (APOmixis-Linked LOcus) gene (apo- and sex-alleles) described by Corral et al [<xref rid="B56-genes-09-00185" ref-type="bibr">56</xref>]. We examined this gene in more detail in our assembly and in other Brassicaseae species. Along with the described copy of <italic>APOLLO</italic>, we also found two other, more distant copies, which evidently arose by two sequential gene duplications (triplication). The <italic>APOLLO</italic> phylogenetic tree may indicate that triplication event occurred before the separation of Brassicaceae species under study (<xref ref-type="fig" rid="genes-09-00185-f004">Figure 4</xref>). We also analyzed the <italic>APOLLO</italic> alleles described in <italic>Boechera ssp</italic>. It was clear that these alleles arose after separation of the <italic>Boechera</italic> genus. In sexual <italic>B. retrofracta</italic> and <italic>B. stricta</italic> polymorphic sites corresponded to the “sexallele”-state and clustered with sex-alleles of the other species.</p><p>These results are compatible with an evolutionary scenario where, after the series of duplications, one of the NEN exonuclease protein (ancestor of <italic>APOLLO</italic>) copies in the common ancestor of <italic>Boechera</italic> spp. experiencing relaxed selection might be deregulated, promoting development of the apomictic reproduction from the ancestral “sexual” state, following by separation of the apomictic lineages. This model of evolution of <italic>APOLLO</italic> alleles might explain the phenomenon of apomictic development in <italic>Boechera</italic> in the diploid condition, emerged as a result of duplication events rather than polyploidy.</p><p>In conclusion, increasing number of sequenced genomes from the economically important Brassicaceae family will facilitate future genetic, genomic, evolutionary, and domestication studies in this family. <italic>B. retrofracta</italic> is thought to be an ancestor of certain hybrids including apomictic species, for example <italic>Boechera divaricarpa</italic>. Consequently, the genome assembly presented in this report may help with the challenging genome assembly of highly heterozygous hybrid <italic>Boechera</italic> species that are apomictic. Thus, the <italic>B. retrofracta</italic> genome reported here will provide a basis to decipher the hybridogenesis events that led to the formation of apomictic <italic>Boechera</italic> accessions.</p></sec></body><back><ack><title>Acknowledgments</title><p>This work was supported by grants 16-54-21014 and 15-54-45001 from the Russian Foundation for Basic Research and by grant 1.52.1647.2016 from St. Petersburg State University (to V.B.), grant IZLRZ3_163885 from the Swiss National Science Foundation (to U.G.) through the Scientific & Technological Cooperation Programme Switzerland-Russia (STCPSR). US National Science Foundation Doctoral Dissertation Improvement Grant 1311269 (to C.R.) and grant R01 GM086496 from the National Institutes of Health (USA) (to T.M.O.). Work conducted by the US Department of Energy Joint Genome Institute was supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. The research was carried out within the framework of the state assignment No. AAAA-A18-118030790063-6 to BIN RAS.</p></ack><notes><title>Author Contributions</title><p>T.M.O., V.B., D.S.R. and U.G. designed the study. T.M.O., C.R., J.S., D.S. and K.P. gathered samples, extracted and sequenced genomic DNA. S.K., A.K., D.Z., E.B. and M.R. performed genome assembly, annotation and phylogenetic analysis. S.K., V.B., M.R., E.B. and R.B. wrote manuscript with revision by all other authors. All authors read and approved the final manuscript.</p></notes><notes notes-type="COI-statement"><title>Conflicts of Interest</title><p>The authors declare no conflict of interest.</p></notes><app-group><app id="app1-genes-09-00185"><title>Appendix A</title><table-wrap id="genes-09-00185-t0A1" orientation="portrait" position="anchor"><object-id pub-id-type="pii">genes-09-00185-t0A1_Table A1</object-id><label>Table A1</label><caption><p>Sequencing scheme of <italic>Boechera retrofracta</italic> genome.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">ID</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Library Type</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Platform</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Read Length</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mean Insert Size (bp)</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Number of Reads Pairs</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">LIB400</td><td align="center" valign="middle" rowspan="1" colspan="1">paired ends</td><td align="center" valign="middle" rowspan="1" colspan="1">Illumina</td><td align="center" valign="middle" rowspan="1" colspan="1">250</td><td align="center" valign="middle" rowspan="1" colspan="1">402</td><td align="center" valign="middle" rowspan="1" colspan="1">189788627</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LIB4000R</td><td align="center" valign="middle" rowspan="1" colspan="1">mate pairs</td><td align="center" valign="middle" rowspan="1" colspan="1">Roche</td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">4014</td><td align="center" valign="middle" rowspan="1" colspan="1">3259085</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LIB5000</td><td align="center" valign="middle" rowspan="1" colspan="1">mate pairs</td><td align="center" valign="middle" rowspan="1" colspan="1">Illumina</td><td align="center" valign="middle" rowspan="1" colspan="1">150</td><td align="center" valign="middle" rowspan="1" colspan="1">4877</td><td align="center" valign="middle" rowspan="1" colspan="1">19083787</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LIB7000</td><td align="center" valign="middle" rowspan="1" colspan="1">mate pairs</td><td align="center" valign="middle" rowspan="1" colspan="1">Illumina</td><td align="center" valign="middle" rowspan="1" colspan="1">150</td><td align="center" valign="middle" rowspan="1" colspan="1">6882</td><td align="center" valign="middle" rowspan="1" colspan="1">34066282</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LIB24000R</td><td align="center" valign="middle" rowspan="1" colspan="1">mate pairs</td><td align="center" valign="middle" rowspan="1" colspan="1">Roche</td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">24,332</td><td align="center" valign="middle" rowspan="1" colspan="1">672098</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BES</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BAC end sequencing</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Sanger</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">147,708</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">17775</td></tr></tbody></table><table-wrap-foot><fn><p>Abbreviations: BAC, bacterial artificial chromosome; BES, BAC end sequencing.</p></fn></table-wrap-foot></table-wrap><fig id="genes-09-00185-f0A1" orientation="portrait" position="anchor"><label>Figure A1</label><caption><p>Pipeline used to assembly genome of <italic>Boechera retrofracta</italic>.</p></caption><graphic xlink:href="genes-09-00185-g0A1"></graphic></fig></app><app id="app2-genes-09-00185"><title>Appendix B</title><p>The original data could be found at: <uri xlink:href="http://public.dobzhanskycenter.ru/ad89dedc8b4674276c9b0760f29b07af/">http://public.dobzhanskycenter.ru/ad89dedc8b4674276c9b0760f29b07af/</uri> or at NCBI, BioProject ID: PRJNA418376.</p></app><app id="app3-genes-09-00185"><title>Appendix C</title><fig id="genes-09-00185-f0C1" orientation="portrait" position="anchor"><label>Figure C1</label><caption><p>Comparison of <italic>Boechera stricta</italic> and <italic>Boechera retrofracta</italic> genomes on a scaffold level.</p></caption><graphic xlink:href="genes-09-00185-g0C1"></graphic></fig></app></app-group><ref-list><title>References</title><ref id="B1-genes-09-00185"><label>1.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Sharbel</surname><given-names>T.F.</given-names></name><name><surname>Mitchell-Olds</surname><given-names>T.</given-names></name></person-group><article-title>Recurrent polyploid origins and chloroplast phylogeography in the <italic>Arabis holboellii</italic> complex (Brassicaceae)</article-title><source>Heredity</source><year>2001</year><volume>87</volume><fpage>59</fpage><lpage>68</lpage><pub-id pub-id-type="doi">10.1046/j.1365-2540.2001.00908.x</pub-id><pub-id pub-id-type="pmid">11678988</pub-id></element-citation></ref><ref id="B2-genes-09-00185"><label>2.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Schranz</surname><given-names>M.E.</given-names></name><name><surname>Dobes</surname><given-names>C.</given-names></name><name><surname>Koch</surname><given-names>M.A.</given-names></name><name><surname>Mitchell-Olds</surname><given-names>T.</given-names></name></person-group><article-title>Sexual reproduction, hybridization, apomixis and polyploidization in the genus <italic>Boechera</italic> (Brassicaceae)</article-title><source>Am. 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Only one major peak at 371× coverage is present, however there are detectable duplications and triplications at 737× and 1120× coverage (upper plot, Y axis is on a logarithmic scale).</p></caption><graphic xlink:href="genes-09-00185-g002"></graphic></fig><fig id="genes-09-00185-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Phylogenetic tree of seven Brassicaceae species used for analysis. Maximum likelihood tree was reconstructed by RAxML using 8959 single copy orthologs and was tested with 1000 bootstrap replicates. Numbers near nodes represent corresponding bootstrap support.</p></caption><graphic xlink:href="genes-09-00185-g003"></graphic></fig><fig id="genes-09-00185-f004" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Phylogenetic tree of the isoforms of <italic>APOLLO</italic> locus (exonuclease NEN) in seven species of interest and alleles of <italic>APOLLO</italic> locus of apomictic <italic>Boechera</italic> species from Corral et al (2013) [<xref rid="B56-genes-09-00185" ref-type="bibr">56</xref>]. Sequences of <italic>Populus trichocarpa</italic>, <italic>Vitus vinifera</italic> and <italic>Glycine max</italic> were used as outgroup. The clade related to the <italic>APOLLO</italic> locus is shown in green, with apo-alleles shown in red. Numbers near nodes represent corresponding bootstrap support.</p></caption><graphic xlink:href="genes-09-00185-g004"></graphic></fig><table-wrap id="genes-09-00185-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t001_Table 1</object-id><label>Table 1</label><caption><p>General statistics for all stages of the assembly pipeline.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Parameter</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Contigs</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Extended Contigs</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Raw Scaffolds</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Intermediate Scaffolfs</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Gap Closed Scaffolds</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Final Scaffolds</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Longest contig</td><td align="center" valign="middle" rowspan="1" colspan="1">791,985</td><td align="center" valign="middle" rowspan="1" colspan="1">792,340</td><td align="center" valign="middle" rowspan="1" colspan="1">8,101,256</td><td align="center" valign="middle" rowspan="1" colspan="1">9,045,706</td><td align="center" valign="middle" rowspan="1" colspan="1">9,049,080</td><td align="center" valign="middle" rowspan="1" colspan="1">9,049,080</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ns</td><td align="center" valign="middle" rowspan="1" colspan="1">28,100</td><td align="center" valign="middle" rowspan="1" colspan="1">28,100</td><td align="center" valign="middle" rowspan="1" colspan="1">11,890,519</td><td align="center" valign="middle" rowspan="1" colspan="1">16,366,994</td><td align="center" valign="middle" rowspan="1" colspan="1">12,409,189</td><td align="center" valign="middle" rowspan="1" colspan="1">12,409,189</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Total length</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">225,649 216</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">226,402,628</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">236,469,041</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">240,945,496</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">241,014,839</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">222,253,471</td></tr></tbody></table></table-wrap><table-wrap id="genes-09-00185-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t002_Table 2</object-id><label>Table 2</label><caption><p>N50 values for all stages of the assembly pipeline and several different cutoffs for minimal scaffold length.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Scaffold Length Cutoff</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Contigs</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Extended Contigs</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Raw Scaffolds</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Intermediate Scaffolfs</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Gap Closed Scaffolds</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Final Scaffolds</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">all</td><td align="center" valign="middle" rowspan="1" colspan="1">85,286</td><td align="center" valign="middle" rowspan="1" colspan="1">84,648</td><td align="center" valign="middle" rowspan="1" colspan="1">1,256,534</td><td align="center" valign="middle" rowspan="1" colspan="1">1,898,006</td><td align="center" valign="middle" rowspan="1" colspan="1">1,898,985</td><td align="center" valign="middle" rowspan="1" colspan="1">2,297,899</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">≥100</td><td align="center" valign="middle" rowspan="1" colspan="1">85,286</td><td align="center" valign="middle" rowspan="1" colspan="1">84,648</td><td align="center" valign="middle" rowspan="1" colspan="1">1,256,534</td><td align="center" valign="middle" rowspan="1" colspan="1">1,898,006</td><td align="center" valign="middle" rowspan="1" colspan="1">1,898,985</td><td align="center" valign="middle" rowspan="1" colspan="1">2,297,899</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">≥250</td><td align="center" valign="middle" rowspan="1" colspan="1">101,388</td><td align="center" valign="middle" rowspan="1" colspan="1">100,393</td><td align="center" valign="middle" rowspan="1" colspan="1">1,442,421</td><td align="center" valign="middle" rowspan="1" colspan="1">2,296,484</td><td align="center" valign="middle" rowspan="1" colspan="1">2,297,899</td><td align="center" valign="middle" rowspan="1" colspan="1">2,297,899</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">≥500</td><td align="center" valign="middle" rowspan="1" colspan="1">115,732</td><td align="center" valign="middle" rowspan="1" colspan="1">115,486</td><td align="center" valign="middle" rowspan="1" colspan="1">1,538,795</td><td align="center" valign="middle" rowspan="1" colspan="1">2,678,857</td><td align="center" valign="middle" rowspan="1" colspan="1">2,680,941</td><td align="center" valign="middle" rowspan="1" colspan="1">2,680,941</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">≥1000</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">122,300</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">121,678</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1,704,064</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2,678,857</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2,680,941</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2,680,941</td></tr></tbody></table></table-wrap><table-wrap id="genes-09-00185-t003" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t003_Table 3</object-id><label>Table 3</label><caption><p>Repeats found by RepeatMasker.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Class</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Number of Elements</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Total Length (bp)</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Fraction of Assembly (%)</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">SINEs</td><td align="center" valign="middle" rowspan="1" colspan="1">577</td><td align="center" valign="middle" rowspan="1" colspan="1">125,298</td><td align="center" valign="middle" rowspan="1" colspan="1">0.06</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LINEs</td><td align="center" valign="middle" rowspan="1" colspan="1">7075</td><td align="center" valign="middle" rowspan="1" colspan="1">4,351,241</td><td align="center" valign="middle" rowspan="1" colspan="1">1.96</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LTR elements</td><td align="center" valign="middle" rowspan="1" colspan="1">51,040</td><td align="center" valign="middle" rowspan="1" colspan="1">40,608,195</td><td align="center" valign="middle" rowspan="1" colspan="1">18.27</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">DNA elements</td><td align="center" valign="middle" rowspan="1" colspan="1">31,638</td><td align="center" valign="middle" rowspan="1" colspan="1">12,868,684</td><td align="center" valign="middle" rowspan="1" colspan="1">5.79</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Unclassified</td><td align="center" valign="middle" rowspan="1" colspan="1">82,693</td><td align="center" valign="middle" rowspan="1" colspan="1">24,363,135</td><td align="center" valign="middle" rowspan="1" colspan="1">10.96</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Total interspersed repeats</td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">82,316,553</td><td align="center" valign="middle" rowspan="1" colspan="1">37.04</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Small RNA</td><td align="center" valign="middle" rowspan="1" colspan="1">5461</td><td align="center" valign="middle" rowspan="1" colspan="1">1,599,354</td><td align="center" valign="middle" rowspan="1" colspan="1">0.72</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Satellites</td><td align="center" valign="middle" rowspan="1" colspan="1">1541</td><td align="center" valign="middle" rowspan="1" colspan="1">573,026</td><td align="center" valign="middle" rowspan="1" colspan="1">0.26</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Simple repeats</td><td align="center" valign="middle" rowspan="1" colspan="1">2044</td><td align="center" valign="middle" rowspan="1" colspan="1">363,642</td><td align="center" valign="middle" rowspan="1" colspan="1">0.16</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Low complexity</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">56</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">7456</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0</td></tr></tbody></table></table-wrap><table-wrap id="genes-09-00185-t004" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t004_Table 4</object-id><label>Table 4</label><caption><p>Results of repeat masking performed by three different tools: RepeatMasker [<xref rid="B32-genes-09-00185" ref-type="bibr">32</xref>], TRF [<xref rid="B34-genes-09-00185" ref-type="bibr">34</xref>], WindowMasker [<xref rid="B35-genes-09-00185" ref-type="bibr">35</xref>].</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Tool</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Number of Repeats</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Total Length (Mbp)</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">RepeatMasker</td><td align="center" valign="middle" rowspan="1" colspan="1">173,023</td><td align="center" valign="middle" rowspan="1" colspan="1">82.31</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">TRF</td><td align="center" valign="middle" rowspan="1" colspan="1">100,593</td><td align="center" valign="middle" rowspan="1" colspan="1">17.41</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Windowmasker</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1,104,650</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">64.20</td></tr></tbody></table></table-wrap><table-wrap id="genes-09-00185-t005" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t005_Table 5</object-id><label>Table 5</label><caption><p>Annotated transfer RNAs (tRNAs).</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">tRNA Type</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Number</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">tRNAs decoding standard 20 AA</td><td align="center" valign="middle" rowspan="1" colspan="1">1126</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Selenocysteine tRNAs (TCA)</td><td align="center" valign="middle" rowspan="1" colspan="1">0</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Possible suppressor tRNAs (CTA,TTA)</td><td align="center" valign="middle" rowspan="1" colspan="1">3</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">tRNAs with undetermined isotypes</td><td align="center" valign="middle" rowspan="1" colspan="1">5</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Resolution of Brassicaceae Phylogeny Using Nuclear Genes<break></break>Uncovers Nested Radiations and Supports Convergent<break></break>Morphological Evolution Predicted pseudogenes</td><td align="center" valign="middle" rowspan="1" colspan="1">32</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Total tRNAs</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1166</td></tr></tbody></table></table-wrap><table-wrap id="genes-09-00185-t006" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t006_Table 6</object-id><label>Table 6</label><caption><p>Annotated ribosomal RNAs (rRNAs).</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">rRNA</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Complete (≥80% of Expected Length)</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Partial (<80% of Expected Length)</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">5.8S</td><td align="center" valign="middle" rowspan="1" colspan="1">178</td><td align="center" valign="middle" rowspan="1" colspan="1">53</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">5S</td><td align="center" valign="middle" rowspan="1" colspan="1">601</td><td align="center" valign="middle" rowspan="1" colspan="1">104</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">28S</td><td align="center" valign="middle" rowspan="1" colspan="1">0</td><td align="center" valign="middle" rowspan="1" colspan="1">1782</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">18S</td><td align="center" valign="middle" rowspan="1" colspan="1">1</td><td align="center" valign="middle" rowspan="1" colspan="1">1458</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">12S</td><td align="center" valign="middle" rowspan="1" colspan="1">0</td><td align="center" valign="middle" rowspan="1" colspan="1">173</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">16S</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">607</td></tr></tbody></table></table-wrap><table-wrap id="genes-09-00185-t007" orientation="portrait" position="float"><object-id pub-id-type="pii">genes-09-00185-t007_Table 7</object-id><label>Table 7</label><caption><p>Comparison of genome characteristics of <italic>Boechera retrofracta</italic> with previously sequenced <italic>Boechera stricta</italic> and <italic>Arabidopsis thaliana</italic> genomes. Source for <italic>B.retrofracta</italic>—this paper, <italic>B.stricta</italic>, <italic>Arabidopsis lyrata</italic> and <italic>A.thaliana</italic>—Phytozome v12.1 database [<xref rid="B57-genes-09-00185" ref-type="bibr">57</xref>].</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Boechera retrofracta</italic></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Boechera stricta</italic> v.1.2</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Arabidopsis lyrata</italic> v2.1</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Arabidopsis thaliana</italic> TAIR10</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Total length</td><td align="center" valign="middle" rowspan="1" colspan="1">227 M</td><td align="center" valign="middle" rowspan="1" colspan="1">184 M</td><td align="center" valign="middle" rowspan="1" colspan="1">207 Mb</td><td align="center" valign="middle" rowspan="1" colspan="1">135 Mb</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chromosomes</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>n</italic> = 7</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>n</italic> = 7</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>n</italic> = 8</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>n</italic> = 5</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Protein-coding loci </td><td align="center" valign="middle" rowspan="1" colspan="1">27,048</td><td align="center" valign="middle" rowspan="1" colspan="1">27,416</td><td align="center" valign="middle" rowspan="1" colspan="1">31,073</td><td align="center" valign="middle" rowspan="1" colspan="1">27,416</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Transcripts</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">28,269</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">29,812</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">33,132</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">35,386</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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