ACHIEVEMENTS OF THE NATIONAL PLANT GENOME INITIATIVE AND NEW HORIZONS IN PLANT BIOLOGY

Committee on the National Plant Genome Initiative: Achievements and Future Directions

Board on Life Sciences

Board on Agriculture and Natural Resources

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

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ACHIEVEMENTS OF THE NATIONAL PLANT GENOME INITIATIVE AND NEW HORIZONS IN PLANT BIOLOGY Committee on the National Plant Genome Initiative: Achievements and Future Directions Board on Life Sciences Board on Agriculture and Natural Resources Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was supported by the Interagency Working Group on Plant Genomes through Contract/ Grant No. DBI-0722206 between the National Academy of Sciences the National Science Foundation and the Department of Energy, Contract/Grant No. 59-0206-7-140 from the U.S. Department of Ag- riculture (USDA) Agricultural Research Service (ARS), Contract/Grant No. 2007-35300-17910 from USDA Cooperative State Research, Education, and Extension Service (CSREES), and Contract/Grant No. 07-DG-11132650-286 from the USDA Forest Service (USFS). The content of this publication does not necessarily reflect the views or policies of the sponsoring agencies, nor does the mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government. International Standard Book Number-13: 978-0-309-11418-9 (Book) International Standard Book Number-10: 0-309-11418-7 (Book) International Standard Book Number-13: 978-0-309-11419-6 (PDF) International Standard Book Number-13: 978-0-309-11419-5 (PDF) Libary of Congress Control Number: 2008923010 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, NW, Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. Cover: Design by Michele de la Menardière. Photo credits: Foreground on the left: Inhibition of RNA silencing pathways in Arabidopsis as shown by false-colored scanning electron micrographs of early-stage flowers from wild-type or silencing-defective plants. Blue flowers are the wild-type. This photo was published on the cover of Developmental Cell, Vol. 4, Issue 2, Copyright Elsevier (2003). Reprinted with permission. Background on the left: Rice field taken during the “Rice Research to Production” course at the In- ternational Rice Research Institute, Los Banos, Philippines in June 2007. Copyright Michael J. Kovach (2007). Reprinted with permission. Right: Soybeans ready for harvest. Photo by Scott Bauer, ARS Photo Unit. Copyright 2008 by the National Academy of Sciences. All rights reserved. Printed in the United States of America.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal govern- ment on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to as- sociate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON THE NATIONAL PLANT GENOME INITIATIVE: ACHIEVEMENTS AND FUTURE DIRECTIONS JEFFERY L. DANGL, Chair, University of North Carolina, Chapel Hill LOIS BANTA, Williams College, Williamstown, MA ROGER BOERMA, University of Georgia, Athens JAMES C. CARRINGTON, Oregon State University, Corvallis JOANNE CHORY, Salk Institute for Biological Studies, San Diego, CA STEVE A. KAY, University of California, San Diego SUZANNA LEWIS, Lawrence Berkeley National Laboratory, Berkeley, CA THOMAS MITCHELL-OLDS, Duke University, Durham, NC NEELIMA R. SINHA, University of California, Davis MICHAEL SNYDER, Yale University, New Haven, CT STEVEN H. STRAUSS, Oregon State University, Corvallis ERIC R. WARD, Two Blades Foundation, Durham, NC Staff EVONNE TANG, Study Director FRANCES E. SHARPLES, Director, Board on Life Sciences ROBIN SCHOEN, Director, Board on Agriculture and Natural Resources MERC FOX, Program Assistant PAULA WHITACRE, Editor v

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BOARD ON LIFE SCIENCES KEITH YAMAMOTO (Chair), University of California, San Francisco ANN M. ARVIN, Stanford University School of Medicine, Stanford, CA RUTH BERKELMAN, Emory University, Atlanta, GA DEBORAH BLUM, University of Wisconsin, Madison VICKI CHANDLER, University of Arizona, Tucson JEFFERY L. DANGL, University of North Carolina, Chapel Hill PAUL R. EHRLICH, Stanford University, Stanford, CA MARK D. FITZSIMMONS, John D. and Catherine T. MacArthur Foundation, Chicago, IL JO HANDELSMAN, University of Wisconsin, Madison KENNETH H. KELLER, University of Minnesota, Minneapolis JONATHAN D. MORENO, University of Pennsylvania Health System, Philadelphia RANDALL MURCH, Virginia Polytechnic Institute and State University, Alexandria MURIEL E. POSTON, Skidmore College, Saratoga Springs, NY JAMES REICHMAN, University of California, Santa Barbara BRUCE W. STILLMAN, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY MARC T. TESSIER-LAVIGNE, Genentech, Inc., South San Francisco, CA JAMES TIEDJE, Michigan State University, East Lansing CYNTHIA WOLBERGER, Johns Hopkins University, Baltimore, MD TERRY L. YATES (deceased), University of New Mexico, Albuquerque Staff FRANCES E. SHARPLES, Director KERRY A. BRENNER, Senior Program Officer ADAM P. FAGEN, Senior Program Officer ANNA FARRAR, Financial Associate MERC FOX, Program Assistant ANN H. REID, Senior Program Officer MARILEE K. SHELTON-DAVENPORT, Senior Program Officer REBECCA WALTER, Senior Program Assistant ROBERT T. YUAN, Senior Program Officer vi

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BOARD ON AGRICULTURE AND NATURAL RESOURCES W. REG GOMES, Chair, University of California, Agriculture and Natural Resources (Emeritus) SANDRA J. BARTHOLMEY, University of Illinois, Chicago ROGER N. BEACHY, Donald Danforth Plant Science Center, St. Louis, MO H.H. CHENG, University of Minnesota (Emeritus), St. Paul DANIEL M. DOOLEY, Dooley Herr & Peltzer, LLP, Visalia, CA JOAN H. EISEMANN, North Carolina State University, Raleigh BRUCE L. GARDNER, University of Maryland, College Park HANS R. HERREN, Millennium Institute, Arlington, VA KIRK C. KLASING, University of California, Davis VICTOR L. LECHTENBERG, Purdue University, West Lafayette, IN BRIAN W. MCBRIDE, University of Guelph, Ontario, Canada ROBERT PAARLBERG, Wellesley College, Watertown, MA BOBBY PHILLS, Florida A&M University, Tallahassee KEITH PITTS, Pew Initiative on Food and Biotechnology, Fair Oaks, CA SONYA SALAMON, University of Illinois, Urbana-Champaign (Emeritus) HAL SALWASSER, Oregon State University, Corvallis PEDRO A. SANCHEZ, The Earth Institute at Columbia University, Palisades, NY NORMAN R. SCOTT, Cornell University, Ithaca, NY BILLIE L. TURNER II, Clark University, Worcester, MA LAURIAN J. UNNEVEHR, University of Illinois, Urbana-Champaign TILAHUN D. YILMA, University of California, Davis Staff ROBIN SCHOEN, Director RUTH S. ARIETI, Senior Program Assistant KAREN L. IMHOF, Administrative Assistant AUSTIN J. LEWIS, Program Officer MICHAEL MA, Visiting Program Officer MARGOT RHYU, Program Assistant JANET MULLIGAN, Research Associate EVONNE TANG, Senior Program Officer PEGGY TSAI, Associate Program Officer vii

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Preface Why should the public and the government care about plant science, let alone the proposition of a National Plant Genome Initiative? Well, quite simply, human life would be impossible without plants. You are likely reading this document wear- ing plant-derived clothing (cotton, or wool from a sheep that ate a plant before shearing), sitting in or on a plant-derived product (wood), and digesting your last meal, made up largely of plants, or something that ate a plant as its last meal before you ate it! And you probably got to work today using transportation that runs on fossil fuel made from plants that lived a couple of hundred million years ago. With- out plants, we’d be in serious trouble. Photosynthesis and carbon sequestration are performed by organisms of all sizes and shapes, from tiny oceanic phytoplankton and single-celled alga, to giant redwood and teak trees, to dense assemblages of diverse plants in rainforest and grassland communities around the planet. Plants and microorganisms, and the communities they form, are fundamental contribu- tors to, and regulators of, the entire earth system. Modern plant biology, then, is about human health and well being, nutrition from new and better foods, fiber and wood production, and renewable alternatives to imported fossil fuels, all of which are produced under the umbrella of respon- sible environmental stewardship. These issues have been focused by the recent broad acceptance that global climate change is upon us, and that human activity contributes to at least some of it. Hence, the imperative to understand plants, how they grow and how they produce the products upon which we all depend, has never been more immediate. Plants are a cornerstone to all animal life, including humans. ix

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Preface x Yet, because we in the United States are no longer an agrarian society, but rather an urban or suburban one with food and fiber surpluses, many of us have lost touch with the simple conceptual notion that plants and plant products remain vital to the way we live. It is also a simple, but profound, truth that plants and plant communities add beauty, flavor, fragrance, and tranquility to our existence. Despite these facts, we, as a society, do not typically consider our reliance on plants, and plant biology, as an important linchpin in U.S. technological and research infrastructure or in our national security, in the same way that we consider public investment in human health research a critical societal priority. For example, the Human Genome Project and the promise of treatments and therapies derived from it have captured the attention of most everyone who watches the news or reads a newspaper. That situation is changing because of the public’s concern with climate change and the recent public interest in alternative and renewable energy sources, includ- ing biofuels. But very few of our constituents make the link between plant genome research and the potential to help generate solutions to the very challenging societal problems that we face. We, as scientists and science policy makers, can do a better job getting that message out. The popular success of books with plant biology and food production as their theme suggests that there is a public interested in plant biology writ large. And, most importantly, our message is compelling on economic competitiveness grounds, on geopolitical grounds, on scientific grounds, and on aesthetic grounds. The National Plant Genome Initiative (NPGI) represents a unique, cross-agen- cy funding enterprise for plant genomics coordinated by the Interagency Working Group (IWG), which is comprised of various federal agencies. As the NPGI ap- proaches its 10-year birthday, the IWG asked the National Research Council (NRC) to evaluate the program and to make recommendations as to how the future of plant genome science might look. The NRC’s Board on Life Sciences and the Board on Agriculture and Natural Resources convened a committee of experts in the fields of plant genetics, epigenetics, informatics, biology education, and molecular and cell biology to evaluate the NPGI program, which involved reviewing the science produced, the science soon to come, and the science that the most creative plant biologists in the country could envision as accomplishments for the NRC report that will be written 20 years from now. The committee did this in the form of a meeting with the IWG, a community workshop, a short questionnaire sent to the more than 270 principal investigators (PIs) who have been funded by NPGI over its first nine years, and a long series of telephone conferences. I would like to thank all the committee members, all the PIs who responded to our questionnaire, and all the participants of the meeting and workshop. We hope that your opinions and advice have been used wisely in this report. NPGI is intertwined unofficially with the National Science Foundation’s other

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Preface xi flagship plant biology activity, the Arabidopsis 2010 Project, which focuses on using a powerful model species to understand many of the basic conceptual aspects of plant growth and development that provide touchstones across at least the flower- ing plants. Hence, NPGI and Arabidopsis 2010 are mentioned together at many junctures in this report. That’s good, and should raise no particular concerns among readers, since the two programs are very complementary and truly syner- gistic. This is easily illustrated in my own discipline, the study of the plant immune system. Over the last 15 years, genetics-based research using Arabidopsis has led to a fairly detailed wiring diagram of the plant immune network. But that diagram benefited from seminal discoveries using flax, tomato, barley, rice, and tobacco. In turn, the conceptual generalities defined in Arabidopsis have subsequently been shown to operate in many other species. Modern molecular, cellular, and developmental biology is the story of the adop- tion of easily manipulated model organisms that serve to provide the “big picture” for a much broader set of scientific truths. Thus, the classic case of research using lab mice and fruit flies that, while of course very compelling in its own right to those scientists who do the work, is easily tied to arguments equating model organism research with breakthroughs in human health. In other words, basic science using animal models has as its ultimate goal explicit betterment of human health. This case is intrinsically more difficult to make for plant science, since we, as humans, use many different plant species for different purposes. The tricky policy issue is how to inform the improvement of many of these plant species using genomics with what will always be limited resources. The multiagency IWG structure of NPGI presented the committee with some problems. For example, it was initially difficult to parse out what is actually funded by NPGI. But the IWG participants in the NPGI worked closely and patiently with the committee over many months to ensure that we had access to the correct sets of data necessary to review both the science and the unique research management concept embodied in the IWG. I hope that this report generates discussion in the research, education, and policy communities. The committee feels strongly that a broad examination of the accomplishments of NPGI and Arabidopsis 2010 Project will be rewarding, and will easily justify rapid growth in federal investment in plant genomics. The case for an expansion of the program is compelling—the infrastructure built over the first nine years of NPGI is in place and now maturing, and the challenges to society that have their solutions in plant science have never been greater. Jeffery L. Dangl Chair, Committee on the National Plant Genome Initiative: Achievements and Future Directions

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Acknowledgments This report is a product of the cooperation and contributions of many people. The members of the committee thank all of the speakers who briefed the commit- tee. (Appendix D presents a list of presentations to the committee.) This report has been reviewed in draft form by persons chosen for their diverse perspectives and technical expertise in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards of objectivity, evidence, and respon- siveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following for their review of this report: James Birchler, University of Missouri Sean Eddy, Janelia Research Farm Michael Herman, Kansas State University Amy Iezzoni, Michigan State University Jan Leach, Colorado State University Michael Lynch, Indiana University Elliot Meyerowitz, California Institute of Technology Ronald Phillips, University of Minnesota Gordon Uno, University of Oklahoma Detlef Weigel, Max Planck Institute for Developmental Biology xiii

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acknowledgments xiv Although the reviewers listed above provided constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations, nor did they see the final draft of the report before its release. The review of this report was overseen by Dr. R. James Cook, Washington State University. Appointed by the National Research Council, Dr. Cook was responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the author committee and the institution.

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Contents SUMMARY 1 1 INTRODUCTION 11 Plant Sciences: Vital to Human Health and Existence, 11 The National Plant Genome Initiative, 15 Study Charge and Scope, 18 2 ASSESSMENT 20 What Is Plant Biology Research in 2007, 20 Scientific and Societal Impacts of NPGI, 21 NPGI and Interagency Cooperation, 47 3 RECOMMENDATIONS AND GOALS: NEW HORIzONS IN PLANT GENOMICS 53 The Future of Plant Genome Research, 53 Tools for Plant Genome Research in the 21st Century, 55 New Horizons in Plant Genome Research, 70 Education and Outreach, 96 GLOSSARY 109 REFERENCES 115 xv

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contents xvi APPENDIXES A Committee Biographies 123 B Publications in Genomics of the Top 40 Most-Cultivated Crops 129 C Questionnaire to Lead Principal Investigators of NPGI Grants 135 D Workshop on the National Plant Genome Initiative 136 E Summary of Grants Given by the National Plant Genome Initiative 139 F List of Websites That Lead Principal Investigators of NPGI Grants Reported as the Top Five Websites Used for NPGI Research 144 G Impact Factor of Journals in Which Awardees of NPGI Grants Published Their Articles 150 H NPGI-Funded K-12 Outreach Activities with Broad Potential Impact 156 I Examples of Joint Call for Proposals and Co-funded Programs by IWG Members 158 J Examples of Interactions with Industry and Plant Breeders Reported by Principal Investigators of NPGI 159 K Tree Genomics or Molecular Genetics Support Provided by the U.S. Department of Agriculture Forest Service 164 L Number and Type of Mutants Distributed by the National Plant Germplasm System 166