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Field Testing Genetically Modified Organisms: Framework for Decisions Committee on Scientific Evaluation of the Introduction of Genetically Modified Microoganisms and Plants into the Environment Board on Biology Commission on Life Sciences National Research Council NATIONAL ACADEMY PRESS Washington, D.C. 1989

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National Academy Press . 2101 Constitution Avenue, N.W. . Washington, D.C 20418 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 report has been reviewed by a group other than the authors according to procedures approved by a Report Review Committee consisting of members of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. 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 government on scientific and technical matters. Dr. frank Press 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. Robert M. White 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. Samuel O. Thier is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy's purposes of furthering knowledge and of 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. Frank Press and Dr. Robert M. White are c}lairman and vice chairman, respectively, of the National Research Council. This study by the Board on Biolo~zv was {ended be the R;~t-~hn~t^~r R^;-n-" Coordinating Committee composed of the Department of Agriculture, Environmental Protection Agency, Food and Drug Administration, National Institutes of Health, and the National Science Foundation, under grants numbers BBS 8820985 and 12-34-30- 0024-GR. _ ~a, ~ Library of Congress Catalog Card Number 89-63061 First Printing September 1989 International Standard Book Number 0-309-04076-0 Second Printing, June 1990 Copyright @) 1989 by the National Academy of Sciences No part of this book may be reproduced by any mechanical, photographic, or electronic process, or in the form of a phonographic recording, nor may it be stored in a retrieval system, transmitted, or otherwise copied for public or private use, without written permission from the publisher, except for the purposes of official use by the United States Government. Printed in the United States of America. First Printing, September 1989 Second Printing, June 1990 Third Printing, March 1992

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COMMITTEE ON SCIENTIFIC EVALUATION OF THE INTRODUCTION OF GENETICALLY MODIFIED MICROORGANISMS AND PLANTS INTO THE ENVIRONMENT Steering Committee Robert H. Burris (Chairman), University of Wisconsin, Madison Fakhri A. Bazzaz, Harvard University, Cambridge, Massachusetts. Ralph W. F. Hardy, BioTechnica/Boyce Thompson, Ithaca, New York Edward L. Korwek, Law Offices of Hogan & Hartson, Washington, D.C. Richard E. Lenski, University of California, Irvine Eugene W. Nester, University of Washington, Seattle Stanley J. Peloquin, University of Wisconsin, Madison Calvin O. Qualset, University of California, Davis Ralph S. Wolfe, University of Illinois, Urbana Subcommittee on Plants Stanley J. Peloquin (Chairman), University of Wisconsin, Madison Roger N. Beachy, Washington University, St. Louis, Missouri Donald N. Duvick, Pioneer Hi-Bred International, ~c., Johnston, Iowa Robert T. Fraley, Monsanto Company, St. Louis, Missouri Ralph W. F. Hardy, BioTechnica/Boyce Thompson, Ithaca, New York Richard N. Mack, Washington State University, Pullman Ann M. Vidaver, University of Nebraska, I,incoIn ... 111

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SUBCOMMITTEE ON MICROORGANISMS Richard E. Lenski (Chairman), University of California, Irvine Peter J. BottornIey, Oregon State University, Corollas Ananda M. Chakrabarty, University of Illinois, Chicago Rita R. Colwell, University of Maryland, College Park Steve K. Fa~rand, University of Illinois, Urbana Robert Haselkorn, University of Chicago Roger D. Milkman, University of Iowa, Iowa City Lu~s Sequeira, University of Wisconsin, Madison James M. Tickle, Michigan State University, East Lansing Board On Biology Staff Alvin G. Lazen, Study Director Clifford Gabriel, Senior Staff Officer Joseph L. Zelibor Jr., Staff Officer Juliette Walker, Administrative Secretary Kathy Marshall, Senior Secretary Caitilin Gordon, Editor 1V

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BOARD ON BIOLOGY Francisco J. Ayala (Chairman), University of California, Irvine Nina V. Fedoroff, Carnegie Institution of Washington, Baltimore, Maryland Timothy H. Goldsmith, Yale University, New Haven, Connecticut Ralph W. F. Hardy, BioTechnica/Boyce Thompson Institute, Ithaca, New York Ernest G. Jaworski, Monsanto Company, St. Louis, Missouri Simon A. Kevin, Cornell University, Ithaca, New York Harold A. Mooney, Stanford University Harold J. Morowitz, George Mason University, Fairfax, Virginia William E. Paul, National Institutes of Health, Washington, D.C. David D. Sabatini, New York University Malcolm S. Steinberg, Princeton University David B. Wake, University of California, Berkeley Bruce M. Alberts (ax-officio), University of California, San Francisco Oskar R. Zaborsky, Director v

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COMMISSION ON LIFE SCIENCES Bruce M. Alberts (Chairman), University of California, San Francisco Perry L. Adkisson, Texas A&M University System, College Station E`rancisco Ayala, University of California, Irvine J. Michael Bishop, University of California Medical Center, San Francisco Freeman J. Dyson, Institute for Advanced Study, Princeton, New Jersey Nina V. Fedoroff, Carnegie Institution of Washington, Baltimore, Maryland Ralph W. F. Hardy, BioTechnica/Boyce Thompson Institute i, Ithaca, New York Richard J. Havel, University of California, San Francisco Leroy E. Hood, California Institute of Technology, Pasadena Donald F. Hornig, Harvard School of Public Health, Boston, Massachusetts Ernest G. Jaworski, Monsanto Company, St. Louis, Missouri Simon A. Levin, Cornell University, Ithaca, New York Harold A. Mooney, Stanford University Steven P. Pakes, University of Texas, Dallas Joseph E. Rall, National Institutes of Health, Bethesda, Maryland Richard D. Remington, University of Iowa, Iowa City Paul G. R:sser, University of New Mexico, Albuquerque Richard Setlow, Brookhaven National Laboratory, Upton, New York Torsten N. Wiesel, Rockefeller University, New York John E. Burris, Executive Director V1

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Preface The potential benefits from the use of genetically modified m~- croorgan~sms and plants are enormous bacteria that biodegrade environmental pollutants, trees that grow more rapidly, food plants that flourish under saline or dry conditions, viruses that control in- sect pests, and a productive and economical agricultural enterprise whose plants use less fertilizer and resist pests. National, state, and local governments are considering safeguards to ensure that such benefits are maximized while possible hazards to the health and wel- fare of humans and damage to the environment are minimized. The necessity exists for timely field research of genetically modified m~- croorgan~sms and plants in environments similar to those ~ which they eventually will be used. A flexible, well-reasoned, scientifically based oversight system must be applied so that tests of genetically modified organisms in the field can proceed when they are deemed safe. Before deciding whether to allow a field test, we are first obliged to define what scientific information and issues must be considered, and then we must ask whether we know enough scientifically to be able to determine the relative safety or risk of the introduction. To obtain a reasoned consensus about these questions, the Biotechnol- ogy Science Coordinating Committee asked the National Academy of Sciences to prepare a report on the introduction of genetically - V11

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modified plants and microorganisms into the environment up to the level of field testing. A steering committee was formed by the National Research Council within the Board on Biology of the Cornrnission on Life Sciences. The steering committee was responsible for the final re- port; two subcommittees also were organized, one concerned with plants and the other with microorganisms, each chaired by a mem- ber of the steering committee but with a membership that extended the expertise available to address the questions in a balanced fashion. Over the past ten months, the committees have grappled with an extensive body of facts, concepts, and opinions and have attempted to formulate a concise, thoughtful, and objective summary that can contribute to resolving the issues. The committees felt their most im- portant task was to reach a consensus about the science surrounding the issues of environmental introductions. Our committees had the luxury of doing this unbound by, but not oblivious to, the existing regulatory principles and approaches that have been applied in this area. The report that follows starts in the middle ~ the sense that the committee has not attempted to write a primer on new technol- ogy, such as recombinant-DNA techniques, nor to provide a detailed background on the biological information that has led to our present level of knowledge. Many other sources provide such information. Rather, we have focused on the issues regarding planned testing of genetically modified plants and micrc~c~r~ni~m~ in the _.. and field. O ~^ ~~~- ~ ~-vie ~ ~ ~ As with all committee-written documents, not every member may agree with every statement. However, the report represents a consensus to which all members agreed. The committee benefited from discussions with members of the Biotechnology Science Coordinating Committee and thanks them and its chairman, Dr. James Wyugaarden, for meeting with the committee and defining the charge. Special thanks are due the chairmen of the subcommittees, Dr. Richard Lenski and Dr. Stanley Peloquin, who graciously accepted an enlarged share of the work load. All members of the committees deserve credit for hewing to the short deadlines. Timely completion of the report would have been impossible without their dedication and concern. Reviewers of the report, though anonymous, deserve thanks for their unportant contribution; they have given close attention to the .. vm

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content, style, and scientific integrity of a report dealing with complex and sometimes contentious issues. Staff members of the Board on Biology and the Commission on Life Sciences were invaluable in their assistance. Dr. John Burris provided wise counsel as the committee work proceeded. Dr. Alvin Lazen, study director, kept the comrn~ttee and staff on the path in pursuit of a finished report. Dr. Clifford Gabriel and Dr. Joseph Zelibor, Jr., guided and coordinated the efforts of the subcommittees on plants and on microorganisms, respectively, and worked closely with the steering committee. Ms. Juliette Walker and Ms. Kathy Marshall skillfully and patiently arranged meetings and handled the administrative and clerical work. We thank Dr. Caitil~n Gordon for her expert editorial assistance in the final stages of writing the report. We sincerely hope that our report will help attain what we ad seek a safe and prudent use of a technology that holds tremendous promise for advancing the welfare of humanity. Robert H. Burris Chairman 1X

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Contents 1 EXECUTIVE SUMMARY 2 INTRODUCTION ,...1 7 The Genetic Modification of Organisms: Merging Classical and Molecular Techniques, 8 Plant Modifications-Classical Techniques, 10 Plot Modifications-Molecular Techniques, 10 Comparison of Classical and Molecular Techniques in Plants, 11 Genome Modification of Microorganisms Classical Techniques, 12 Genome Modification of Microorganisms Molecular Techniques, 13 Comparison of Classical and Molecular Techniques In Microoorganisms, 13 Summary, 14 3 PAST EXPERIENCE WITH GENETIC MODIFICATION OF PLANTS AND THEIR INTRODUCTION INTO THE ENVIRONMENT................................. Types of Genetic Modification in Plants, 18 The Results of Genetic Modification, 20 X1 16

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Modifications and Their Effects on Persistence, 21 Case Studies of Introduced Crops, 24 Past Experience with Confinement, 32 Summary Points, 36 4 ENHANCED WEEDINESS: A MAJOR ENVIRONMENTAL ISSUE General Principles, 37 The Relationship Between the Introduction of Exotic Plants and Genetically Modified Plants, 39 The Ability of Crops to Revert to a Wild or Weedy Condition, 42 Hybridization Between Crops and Their Wild Relatives, 43 Summary Points, 53 5 PAST EXPERIENCE WITH THE INTRODUCTION OF MODIFIED PLANTS: MOLECULAR GENETIC TECHNIQUES .... e - - - - - - - - - - - - - ~ ~ - - - - - e e - - e e e - - - - - - e e - - Properties of Molecular Genetic Modifications, 55 Case Studies of Plants Modified by Molecular Genetic Techniques, 59 Summary Points, 64 6 CONCLUSIONS AND RECOMMENDATIONS: PLANTS e e e - ~ - e e e e e e e e e e ~ e e e e e ~ - - - - - - - ~ e e ~ What Does Past Experience Teach Us?, 66 Control and Confinement of Genetically Modified Plant Varieties, 68 Large-Scale Introductions and Commercialization, 69 A Framework for Assessing Risk, 70 Geographic Frame of Reference, 74 Oversight Considerations, 76 54 ...65 7 PAST EXPERIENCE WITH THE INTRODUCTION OF MICROORGANISMS INTO THE ENVIRONMENT 77 History of Beneficial Uses of Microorganisms and Prospects for the Future, 77 Similarities and Differences Between Classical and Molecular Methods, 83 . X11

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Considerations Associated with Unfamiliar Applications of Microorganisms, 84 Summary Points, 85 8 PROPERTIES OF THE GENETIC MODI1?ICATION History, 87 Genetic Considerations, 89 Summary Points, 97 9 PHENOTYPIC PROPERTIES OF SOURCE MICROORGANISMS AND THEIR GENETICALLY MODIFIED DERIVATIVES ............................ Persistence, 99 Phenotypic Properties Affecting the Ecosystem, 102 Characteristics of Microbial Pathogens, 105 General Phenotypic Characteristics of Pathogens, 108 Summary Points, 111 10 PROPERTIES OF THE ENVIRONMENT RELEVANT TO THE INTRODUCTION OF GENETICALLY MODIFIED MICROORGANISMS.......................... Types of Environments, 113 Habitability of Environments, 114 Disperse, 115 Suitability of Microcosms for Testing of Microbial Introductions, 117 Scale and frequency of Introduction, 119 Potential Effectiveness of Monitoring, 119 Mitigation, 120 Summary Points, 121 11 CONCLUSIONS AND RECOMMENDATIONS: MICROORGANISMS .................. APPENDS Historical Overview of Nucleic Acid Bic~ter~ology: 1973 to 1989.............. LITERATURE CITED.. INFORMATION ON COMMITTEE MEMBERS -- X111 ....... 86 ...... 99 113 123 ..133 .143 165

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