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The B73 Maize Genome: Complexity, Diversity, and Dynamics

Patrick S. Schnable, Doreen Ware, Robert S. Fulton, Joshua C. Stein, Fusheng Wei, Shiran Pasternak, Chengzhi Liang, Jianwei Zhang, Lucinda Fulton, Tina A. Graves, Patrick Minx, Amy Denise Reily, Laura Courtney, Scott S. Kruchowski, Chad Tomlinson, Cindy Strong, Kim Delehaunty, Catrina Fronick, Bill Courtney, Susan M. Rock, Eddie Belter, Feiyu Du, Kyung Kim, Rachel M. Abbott, Marc Cotton, Andy Levy, Pamela Marchetto, Kerri Ochoa, Stephanie M. Jackson, Barbara Gillam, Weizu Chen, Le Yan, Jamey Higginbotham, Marco Cardenas, Jason Waligorski, Elizabeth Applebaum, Lindsey Phelps, Jason Falcone, Krishna Kanchi, Thynn Thane, Adam Scimone, Nay Thane, Jessica Henke, Tom Wang, Jessica Ruppert, Neha Shah, Kelsi Rotter, Jennifer Hodges, Elizabeth Ingenthron, Matt Cordes, Sara Kohlberg, Jennifer Sgro, Brandon Delgado, Kelly Mead, Asif Chinwalla, Shawn Leonard, Kevin Crouse, Kristi Collura, Dave Kudrna, Jennifer Currie, Ruifeng He, Angelina Angelova, Shanmugam Rajasekar, Teri Mueller, Rene Lomeli, Gabriel Scara, Ara Ko, Krista Delaney, Marina Wissotski, Georgina Lopez, David Campos, Michele Braidotti, Elizabeth Ashley, Wolfgang Golser, HyeRan Kim, Seunghee Lee, Jinke Lin, Zeljko Dujmic, Woojin Kim, Jayson Talag, Andrea Zuccolo, Chuanzhu Fan, Aswathy Sebastian, Melissa Kramer, Lori Spiegel, Lidia Nascimento, Theresa Zutavern, Beth Miller, Claude Ambroise, Stephanie Muller, Will Spooner, Apurva Narechania, Liya Ren, Sharon Wei, Sunita Kumari, Ben Faga, Michael J. Levy, Linda McMahan, Peter Van Buren, Matthew W. Vaughn, Kai Ying, Cheng-Ting Yeh, Scott J. Emrich, Yi Jia, Ananth Kalyanaraman, An-Ping Hsia, W. Brad Barbazuk, Regina S. Baucom, Thomas P. Brutnell, Nicholas C. Carpita, Cristian Chaparro, Jer-Ming Chia, Jean-Marc Deragon, James C. Estill, Yan Fu, Jeffrey A. Jeddeloh, Yujun Han, Hyeran Lee, Pinghua Li, Damon R. Lisch, Sanzhen Liu, Zhijie Liu, Dawn Holligan Nagel, Maureen C. McCann, Phillip SanMiguel, Alan M. Myers, Dan Nettleton, John Nguyen, Bryan W. Penning, Lalit Ponnala, Kevin L. Schneider, David C. Schwartz, Anupma Sharma, Carol Soderlund, Nathan M. Springer, Qi Sun, Hao Wang, Michael Waterman, Richard Westerman, Thomas K. Wolfgruber, Lixing Yang, Yeisoo Yu, Lifang Zhang, Shiguo Zhou, Qihui Zhu, Jeffrey L. Bennetzen, R. Kelly Dawe, Jiming Jiang, Ning Jiang, Gernot G. Presting, Susan R. Wessler, Srinivas Aluru, Robert A. Martienssen, Sandra W. Clifton, W. Richard McCombie, Rod A. Wing, and Richard K. Wilson [email protected]Authors Info & Affiliations
Science
20 Nov 2009
Vol 326, Issue 5956
pp. 1112-1115

A-Maize-ing

Maize is one of our oldest and most important crops, having been domesticated approximately 9000 years ago in central Mexico. Schnable et al. (p. 1112; see the cover) present the results of sequencing the B73 inbred maize line. The findings elucidate how maize became diploid after an ancestral doubling of its chromosomes and reveals transposable element movement and activity and recombination. Vielle-Calzada et al. (p. 1078) have sequenced the Palomero Toluqueño (Palomero) landrace, a highland popcorn from Mexico, which, when compared to the B73 line, reveals multiple loci impacted by domestication. Swanson-Wagner et al. (p. 1118) exploit possession of the genome to analyze expression differences occurring between lines. The identification of single nucleotide polymorphisms and copy number variations among lines was used by Gore et al. (p. 1115) to generate a Haplotype map of maize. While chromosomal diversity in maize is high, it is likely that recombination is the major force affecting the levels of heterozygosity in maize. The availability of the maize genome will help to guide future agricultural and biofuel applications (see the Perspective by Feuillet and Eversole).

Abstract

We report an improved draft nucleotide sequence of the 2.3-gigabase genome of maize, an important crop plant and model for biological research. Over 32,000 genes were predicted, of which 99.8% were placed on reference chromosomes. Nearly 85% of the genome is composed of hundreds of families of transposable elements, dispersed nonuniformly across the genome. These were responsible for the capture and amplification of numerous gene fragments and affect the composition, sizes, and positions of centromeres. We also report on the correlation of methylation-poor regions with Mu transposon insertions and recombination, and copy number variants with insertions and/or deletions, as well as how uneven gene losses between duplicated regions were involved in returning an ancient allotetraploid to a genetically diploid state. These analyses inform and set the stage for further investigations to improve our understanding of the domestication and agricultural improvements of maize.

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Information & Authors

Information

Published In

Science
Volume 326 | Issue 5956
20 November 2009

Submission history

Received: 1 July 2009
Accepted: 13 October 2009
Published in print: 20 November 2009

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Acknowledgments

The Maize Genome Sequencing Project supported by NSF award DBI-0527192 (R.K.W., S.W.C., R.S.F., R.A.W., P.S.S., S.A., L.S., D.W., W.R.M., R.A.M.). The Maize Transposable Element Consortium and the Maize Centromere Consortium supported by NSF awards DBI-0607123 (S.R.W., J.L.B., R.K.D., N.J., P.S.M.) and DBI-0421671 (R.K.D., J.J., G.G.P.). Also supported by NSF grants DBI-0321467 (D.W.), DBI-0321711 (P.S.S.), DBI-0333074 (D.W.), DBI-0501818 (D.C.S.), DBI-0501857 (Y.Y.), DBI-0701736 (T.P.B., Q.S.), DBI-0703273 (R.A.M.), and DBI-0703908 (D.W.), and by USDA National Research Initiative Grants 2005-35301-15715 and 2007-35301-18372 from the USDA Cooperative State Research, Education, and Extension Service (P.S.S.) and from the USDA-ARS (408934 and 413089) to D.W., and from the Office of Science (Biological and Environmental Research), U.S. Department of Energy, grant DE-FG02-08ER64702 to N.C.C. and M.C.M. Sequences of the reference chromosomes have been deposited in GenBank as accession numbers CM000777 to CM000786. RNA-sequence reads have been deposited in the Gene Expression Omnibus (GEO) database (www.ncbi.nlm.nih.gov/geo) as accession numbers GSE16136, GSE16868, and GSE16916. Centromeric sequences have been deposited in the National Center for Biotechnology Information, NIH, Trace Archive as accessions 1757396377 to 1757412600 and 2185189231 to 2185200942.

Authors

Affiliations

Patrick S. Schnable*
Center for Plant Genomics, Iowa State University, Ames, IA 50011, USA.
Department of Agronomy, Iowa State University, Ames, IA 50011, USA.
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA.
Center for Carbon Capturing Crops, Iowa State University, Ames, IA 50011, USA.
Doreen Ware*
U.S. Department of Agriculture (USDA), North Atlantic Area, Robert Holley Center for Agriculture and Health, Ithaca, NY 14853, USA.
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Robert S. Fulton
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Joshua C. Stein
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Fusheng Wei
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Shiran Pasternak
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Chengzhi Liang
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Jianwei Zhang
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Lucinda Fulton
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Tina A. Graves
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Patrick Minx
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Amy Denise Reily
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Laura Courtney
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Scott S. Kruchowski
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Chad Tomlinson
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Cindy Strong
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kim Delehaunty
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Catrina Fronick
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Bill Courtney
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Susan M. Rock
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Eddie Belter
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Feiyu Du
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kyung Kim
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Rachel M. Abbott
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Marc Cotton
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Andy Levy
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Pamela Marchetto
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kerri Ochoa
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Stephanie M. Jackson
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Barbara Gillam
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Weizu Chen
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Le Yan
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jamey Higginbotham
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Marco Cardenas
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jason Waligorski
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Elizabeth Applebaum
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Lindsey Phelps
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jason Falcone
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Krishna Kanchi
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Thynn Thane
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Adam Scimone
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Nay Thane
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jessica Henke
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Tom Wang
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jessica Ruppert
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Neha Shah
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kelsi Rotter
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jennifer Hodges
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Elizabeth Ingenthron
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Matt Cordes
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Sara Kohlberg
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Jennifer Sgro
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Brandon Delgado
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kelly Mead
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Asif Chinwalla
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Shawn Leonard
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kevin Crouse
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Kristi Collura
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Dave Kudrna
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Jennifer Currie
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Ruifeng He
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Angelina Angelova
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Shanmugam Rajasekar
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Teri Mueller
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Rene Lomeli
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Gabriel Scara
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Ara Ko
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Krista Delaney
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Marina Wissotski
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Georgina Lopez
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
David Campos
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Michele Braidotti
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Elizabeth Ashley
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Wolfgang Golser
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
HyeRan Kim
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Seunghee Lee
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Jinke Lin
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Zeljko Dujmic
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Woojin Kim
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Jayson Talag
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Andrea Zuccolo
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Chuanzhu Fan
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Aswathy Sebastian
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Melissa Kramer
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Lori Spiegel
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Lidia Nascimento
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Theresa Zutavern
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Beth Miller
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Claude Ambroise
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Stephanie Muller
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Will Spooner
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Apurva Narechania
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Liya Ren
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Sharon Wei
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Sunita Kumari
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Ben Faga
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Michael J. Levy
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Linda McMahan
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Peter Van Buren
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Matthew W. Vaughn
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Kai Ying
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA.
Cheng-Ting Yeh
Center for Plant Genomics, Iowa State University, Ames, IA 50011, USA.
Department of Agronomy, Iowa State University, Ames, IA 50011, USA.
Scott J. Emrich
Department of Electrical and Computer Engineering, Iowa State University, Ames, IA 50011, USA.
Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556, USA.
Yi Jia
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA.
Ananth Kalyanaraman
Department of Electrical and Computer Engineering, Iowa State University, Ames, IA 50011, USA.
School of Electrical Engineering and Computer Science, Washington State University, Pullman, WA 99164, USA.
An-Ping Hsia
Center for Plant Genomics, Iowa State University, Ames, IA 50011, USA.
Department of Agronomy, Iowa State University, Ames, IA 50011, USA.
W. Brad Barbazuk
Department of Botany, University of Florida, Gainesville, FL 32611, USA.
Regina S. Baucom
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Thomas P. Brutnell
Boyce Thompson Institute, Cornell University, Ithaca, NY 14853, USA.
Nicholas C. Carpita
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA.
Cristian Chaparro
Université de Perpignan Via Domitia, CNRS, Perpignan, France.
Jer-Ming Chia
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Jean-Marc Deragon
Université de Perpignan Via Domitia, CNRS, Perpignan, France.
James C. Estill
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Yan Fu
Department of Agronomy, Iowa State University, Ames, IA 50011, USA.
Center for Carbon Capturing Crops, Iowa State University, Ames, IA 50011, USA.
Jeffrey A. Jeddeloh
NimbleGen, Madison, WI 53711, USA.
Yujun Han
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Hyeran Lee
Department of Horticulture, University of Wisconsin–Madison, Madison, WI 53706, USA.
Pinghua Li
Boyce Thompson Institute, Cornell University, Ithaca, NY 14853, USA.
Damon R. Lisch
Department of Plant Biology, University of California, Berkeley, CA, 94720, USA.
Sanzhen Liu
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA.
Zhijie Liu
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Dawn Holligan Nagel
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Maureen C. McCann
Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA.
Phillip SanMiguel
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.
Alan M. Myers
Department of Biochemistry, Biophysics, and Molecular Biology, Iowa State University, Ames, IA, 50011, USA.
Dan Nettleton
Department of Statistics, Iowa State University, Ames, IA 50011, USA.
John Nguyen
Departments of Mathematics, Biology, and Computer Science, University of Southern California, Los Angeles, CA 90089, USA.
Bryan W. Penning
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA.
Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA.
Lalit Ponnala
Cornell University Computational Biology Service Unit, Cornell University, Ithaca, NY 14850, USA.
Kevin L. Schneider
Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, HI 96822, USA.
David C. Schwartz
Laboratory for Molecular and Computational Genomics, Department of Chemistry, Laboratory of Genetics, University of Wisconsin–Madison, Madison, WI 53706, USA.
Anupma Sharma
Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, HI 96822, USA.
Carol Soderlund
BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Nathan M. Springer
Department of Plant Biology, University of Minnesota, St. Paul, MN 55108, USA.
Qi Sun
Cornell University Computational Biology Service Unit, Cornell University, Ithaca, NY 14850, USA.
Hao Wang
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Michael Waterman
Departments of Mathematics, Biology, and Computer Science, University of Southern California, Los Angeles, CA 90089, USA.
Richard Westerman
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA.
Thomas K. Wolfgruber
Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, HI 96822, USA.
Lixing Yang
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Yeisoo Yu
BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Lifang Zhang
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Shiguo Zhou
Laboratory for Molecular and Computational Genomics, Department of Chemistry, Laboratory of Genetics, University of Wisconsin–Madison, Madison, WI 53706, USA.
Qihui Zhu
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Jeffrey L. Bennetzen
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
R. Kelly Dawe
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Jiming Jiang
Department of Horticulture, University of Wisconsin–Madison, Madison, WI 53706, USA.
Ning Jiang
Department of Horticulture, Michigan State University, East Lansing, MI 48824, USA.
Gernot G. Presting
Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, HI 96822, USA.
Susan R. Wessler
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.
Srinivas Aluru
Center for Plant Genomics, Iowa State University, Ames, IA 50011, USA.
Department of Electrical and Computer Engineering, Iowa State University, Ames, IA 50011, USA.
Indian Institute of Technology, Bombay, India.
Robert A. Martienssen
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Sandra W. Clifton
The Genome Center at Washington University, St. Louis, MO 63108, USA.
W. Richard McCombie
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Rod A. Wing
Arizona Genomics Institute, School of Plant Sciences and Department of Ecology and Evolutionary Biology, BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ 85721, USA.
Richard K. Wilson [email protected]
The Genome Center at Washington University, St. Louis, MO 63108, USA.
Department of Genetics, Washington University School of Medicine, St. Louis, MO 63110, USA.

Notes

*
These authors contributed equally to this work.
These authors contributed equally to data production and analysis.
To whom correspondence should be addressed. E-mail: [email protected]

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