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OPPORTUNITI B10 IN ~ GY Committee on Research Opportunities in Biology Board on Biology Commission on Life Sciences National Research Council NATIONAL ACADEMY PRESS Washington, D.C. 1989

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COMMITTEE ON RESEARCH OPPORTUNITIES IN BIOLOGY PETER H. RAVEN (Chairman), Missouri Botanical Garden, St. Louis CHARLES R. CANTOR, Columbia University College of Physicians and Surgeons, New York, New York W. MAXWELL COWAN, Howard Hughes Medical Institute, Bethesda, Maryland JAMES D. EBERT, Johns Hopkins University, Baltimore, Maryland THOMAS EISNER, Cornell University, Ithaca, New York GERALD R. FINK, Whitehead Institute and Massachusetts Institute of Technology, Cambridge WILFORD R. GARDNER, University of California, Berkeley DANIEL HARTL, Washington University School of Medicine, St. Louis, Missouri LEROY HOOD, California Institute of Technology, Pasadena ERNEST G. JAWORSKI, Monsanto Company, St. Louis, Missouri ERIC R. KANDEL, Columbia University College of Physicians and Surgeons and Howard Hughes Medical Institute, New York, New York HANS KENDE, Michigan State University, East Lansing GEORGE R. PALADE, Yale University School of Medicine, New Haven, Connecticut MARY-LOU PARDUE, Massachusetts Institute of Technology, Cambridge WILLIAM E. PAUL, National Institutes of Health, Bethesda, Maryland THOMAS D. POLLARD, Johns Hopkins Medical School, Baltimore, Maryland RUSSELL ROSS, University of Washington School of Medicine, Seattle MELVIN I. SIMON, California Institute of Technology, Pasadena DONALD F. STEINER, University of Chicago, Illinois EDWARD O. WILSON, Harvard University, Cambridge, Massachusetts NRC Staff JOHN E. BURRIS, Study Director CLIFFORD J. GABRIEL, Senior Program Officer DAVID J. POLICANSKY, Senior Program Officer (through December 1986) WALTER G. ROSEN, Senior Program Officer (through December 1986) CAITILIN GORDON, Editor M. FRANCES WALTON, Administrative Secretary (through August 1988) KATHY L. MARSHALL, Senior Secretary . ~

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Panel on Cell Organization THOMAS POLLARD (Co-chairman), Johns Hopkins Medical School, Baltimore, Maryland BRUCE ALBERTS (Co-cha~rman), University of California, San Francisco THOMAS DEUEL, Jewish Hospital at Washington University Medical Center, St. Louis, Missouri LELAND HARTWELL, University of Washington, Seattle PHILLIP SHARP, Massachusetts Institute of Technology, Cambridge Panel on Ecology and Ecosystems SIMON LEVIN (Chairman), Cornell University, Ithaca, New York JAMES EHLERINGER, University of Utah, Salt Lake City THOMAS EISNER, Cornell University, Ithaca, New York STEPHEN HUBBELL, University of Iowa, Iowa City HOLGER JANNASCH, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts PETER RAVEN, Missouri Botanical Garden, St. Louis THOMAS SCHOENER, University of California, Davis PETER V1TOUSEK, Stanford University, Stanford, California Panel on Evolution and Diversity DANIEL HARTL (Co-chairr~n), Washington University School of Medicine, St. Louis, Missouri MICHAEL CLEGG (Co-chairman), University of California, Riverside J. WILLIAM SCHOPF, University of California, Los Angeles DOUGLAS FUTUYMA, State University of New York at Stony Brook DAVID RAUP, University of Chicago, Illinois EDWARD WILSON, Harvard University, Cambridge, Massachusetts CARL WOESE, University of Illinois, Urbana Panel on Genome Organization and Expression GERALD FINK (Co-chairman), Whitehead Institute and Massachusetts Institute of Technology, Cambridge JOSEPH GALL (Co-chcurman), Carnegie Institution of Washington, Baltimore, Maryland PETER QUAIL, Plant Gene Expression Center, Albany, California MELVIN SIMON, California Institute of Technology, Pasadena JOAN STERN, Yale University School of Medicine, New Haven, Connecticut RAYMOND WHITE, Howard Hughes Medical Institute and University of Utah Medical School, Salt Lake City IV

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Panel on Growth and Development MARY-LOU PARDUE (Co-cha~rman), Massachusetts Institute of Technology, Cambridge MARC KIRSCHNER (Co-chairman), University of California Medical School, San Francisco SUSAN BRYANT, University of California, Vine COREY GOODMAN, University of California, Berkeley PHILIPPA MARRACK, National Jewish Hospital, Denver, Colorado DAVOR SOLTER, Wistar Institute, Philadelphia, Pennsylvania Panel on Immune System, Pathogens, and Host Defenses WILLIAM PAUL (Co-chairman), National Institutes of Health, Bethesda, Maryland BERNARD FIELDS (Co-chairman), Harvard Medical School, Boston, Massachusetts ZANVIL COHN, Rockefeller University, New York, New York STANLEY FALKOW, Stanford University, Stanford, California MALCOLM GEFTER, Massachusetts Institute of Technology, Cambridge DAVID SACHS, National Institutes of Health, Bethesda, Maryland MATTHEW SCHARFF, Albert Einstein College of Medicine, New York, New York THOMAS WALDMANN, National Institutes of Health, Bethesda, Maryland Panel on Integrative Approaches to Organism Function and Disease RUSSELL ROSS (Chairman), University of Washington, Seattle HENRY BOURNE, University of California, San Francisco MICHAEL CZECH, University of Massachusetts Medical School, Worcester FRED FOX, University of California, Los Angeles BERTIL HILLE, University of Washington School of Medicine, Seattle PHILIP NEEDLEMAN, Washington University, St. Louis, Missouri ALEXANDER NICHOLS, University of California, Berkeley Panel on Molecular Structure and Function CHARLES CANTOR (Co-chairman), Columbia University College of Physicians and Surgeons, New York, New York FREDERICK RICHARDS (Co-chairman), Guilford, Connecticut MARK PTASHNE, Harvard University, Cambridge, Massachusetts LUBERT STAYER, Stanford Medical School, Stanford, California NIGEL UNWIN, Stanford University, Stanford, California DONALD WILEY, Harvard University, Cambridge, Massachusetts v

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Panel on Neurobiology and Behavior W. MAXWELL COWAN (Co-chairman), Howard Hughes Medical Institute, Bethesda, Maryland ERIC KANDEL (Co-chairman), Columbia University College of Physicians and Surgeons and Howard Hughes Medical Institute, New York, New York ALBERT AGUAYO, Montreal General Hospital, Canada EMILIO BlZ/.l, Massachusetts Institute of Technology, Cambridge JOHN DOWLING, Harvard University, Cambridge, Massachusetts GERALD FISCHBACH, Washington University School of Medicine, St. Louis, Missouri BERT HOLLDOBLER, Harvard University, Cambridge, Massachusetts MICHAEL POSNER, University of Oregon, Eugene SOLOMON SNYDER, Johns Hopkins University School of Medicine, Baltimore, Maryland Panel on New Technology and Industrial Biotechnology ERNEST JAWORSKI (Co-chairman), Monsanto Company, St. Louis, Missouri LEROY HOOD (Co-chairman), California Institute of Technology, Pasadena RITA COLWELL, University of MaIyland, College Park CHARLES COONEY, Massachusetts Institute of Technology, Cambridge ROBERT KAMEN, Genetics Institute, Cambridge, Massachusetts ROBERT SHULMAN, Yale University, New Haven, Connecticut Panel on Plant Biology and Agriculture HANS KENDE (Co-chairman), Michigan State University, East Lansing WILFORD GARDNER (Co-chairman), University of California, Berkeley JOHN BOYER, University of Delaware, Lewes TSUNE KOSUGE (deceased), University of California, Davis SHARON LONG, Stanford University, Sanford, California DONALD ORT, USDA-AAS-University of Illinois, Urbana Vl

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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, Boyce Thompson Institute of Plant Research, Ithaca, New York ERNEST G. JAWORSKI, Monsanto Company, St. Louis, Missouri SIMON A. LEVIN, Cornell University, Ithaca, New York HAROLD A. MOONEY, Stanford University, Stanford, California HAROLD J. MOROW1'I Z. George Mason University, Fairfax, Virginia MARY-LOU PARDUE, Massachusetts Institute of Technology, Cambridge WILLIAM E. PAUL, National Institutes of Health, Bethesda, Maryland DAVID D. SABAT1NI, New York University, New York MICHAEL E. SOULE, University of Michigan, Ann Arbor MALCOLM S. STEINBERG, Princeton University, Princeton, New Jersey DAVID B. WAKE, University of California, Berkeley BRUCE M. ALBERTS (0~-officio), University of California, San Francisco NRC Staff JOHN E. BURRIS, Executive Director, Commission on Life Sciences . v``

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COMMISSION ON LIFE SCIENCES BRUCE M. ALBERTS (Chairman), University of California, San Francisco PERRY L. ADKISSON, The Texas A&M University System, College Station, Texas FRANCISCO J. AYALA, University of Califomia, 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, Boyce Thompson Institute of Plant Research, Ithaca, New York RICHARD J. HAVEL, University of California School of Medicine, 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, Stanford, California STEVEN P. PAKES, University of Texas Southwestern Medical School, Dallas JOSEPH E. RALL, National Institutes of Health, Bethesda, Maryland RICHARD D. REMINGTON, University of Iowa, Iowa City PAUL G. RISSER, University of New Mexico, Albuquerque RICHARD B. SETLOW, Brookhaven National Laboratory, Upton, New York TORSTEN N. WIESEL, Rockefeller University, New York, New York NRC Stay JOHN E. BURRIS, Executive Director .. . Vli!

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Acknowledgments The committee would like to acknowledge the thoughtful work of the contribu- tors and reviewers: Edward Adelberg Bruce Baker Edwin Beachey Roger Beachy Hans Bode Lawrence Bogorad Marianne Bonner-Fraser Dan Brower Bob Buchanan Guy Bush Judith Campbell Thomas Cech Robert Chanock Bruce Chesebro Tom Cline C. Robert Cloninger R. John Collier Robert J. Collier John Collins Jonathon Cooke George Cross Kathryn Crossin Deborah Delmer William Earnshaw Robert Fraley Michael Freeling Larry Gerace Norton Gilula Timothy Goldsmith Leslie Gottlieb Antonio Gotto J. Frederick Grassle Paul Green Douglas Hanahan Richard Harlan George Haughn Ari Helenius Samuel Hellman John Hildebrand H. Robert Horvitz Rudolf Jaenisch ~y Kahn Arthur Kelman Eric Knudsen Thomas Kornberg Stephen Krane ~x Michael Levine Jane Lubchenco Harry MacWiD~s Thomas Maniatis Lynn Margulis Paul Marks David Martin Gail Martin Victor McKusick Douglas Melton Harold Mooney J. Anthony Movshon Howard Nash June Nasrallah Daniel Nathans Stephen O'Brien William Ogren Michael Oldstone Gordon Orians David Page David Pisetsky Peter Quail Calvin Quate

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ACKNOWLEl)GME7VTS Richard Root Michael Rosenzweig John Roth Erkki Ruoslahti Frank Ruddle Jay Savage Luis Sequeira David Schlessinger James Schwartz Matthew Scott Michael Sheetz Emil Skamene Allan Spradling Malcolm Steinberg William Sugden James Tavares D. Lansing Taylor Howard Temin Samuel Thier Robert Trelstad David Van Essen Graham Walker David Wake Allan Wilson Thomas Woolsey

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Preface In 1970 the National Research Council published Biology and the Future of Man. This report, edited by Philip Handler, then president of the National Acad- emy of Sciences, summarized the state of biology at that time. Now, almost 20 years later, the National Research Council, with the publication of this report, reevaluates research opportunities in biology and attempts to convey the current excitement in the field of biology. Our report differs from Biology and the Future of Man because of the enormous advances that have occurred in biology over the past two decades. The field has, in fact, changed to the point that no single individual can hope to grasp all of the new activities and opportunities. To address this daunting task, a committee of distinguished scientists began in late 1985 to determine the major research areas that exist in the field of biology and then to discuss how advances in each of these areas can be maximized and how and where possible interactions among biologists of various subdisciplines and biologists and other scientists can be facilitated to lead to new interdiscipli- nary insights and approaches. This committee of 20 individuals soon realized that such a goal would require the assistance of many other experts. Toward this end the committee organized 11 panels, each with at least one individual from the committee. Each panel was asked to produce a report of about 50 pages stressing the current and future opportunities for exciting research in their area of expertise and also to stress the interconnections of biological scientists with others from different areas of biology and from other disciplines. Even the panels found that they needed assistance; thus the input of additional individuals was solicited for the report. The steering committee edited these reports, in some cases combining the efforts of several groups to produce a single chapter, in other instances letting panel topics stand as chapters in the final report. The committee report then

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. . xzz PREFACE underwent an extensive review process. The reviewers' comments were ex- tremely useful to the committee in polishing and producing the final draft of the report. This report reflects the panoply of interesting and exciting topics that consti- tute biology. Some areas are barely covered and still others not at all. This is by necessity: There is just too much information today in biology, a fact illustrated by the length of high school and college introductory textbooks that can character- istically exceed 1,000 pages. In selecting areas to be included we chose those that represent major themes in biological research. In many cases such selections were difficult, since most of biology today is expanding as new techniques and ideas are applied to old fields or to new areas. We have produced this volume for a large audience: biologists; policymakers both in government, universities, and in industry; and other scientists from a variety of disciplines who may interact with biologists. We hope that each of these groups will learn from this book. For all of you who read this report, our goal is to leave you with some understanding and appreciation of the diversity of problems and opportunities that await the biologist. Some of these opportunities will provide us with a better understanding of the basic workings of life, and others will have immediate application in our lives through medicine, agriculture, or environmental management. In any such effort it is important to acknowledge the work of the many individuals, in addition to the committee members, who contributed to this effort. Those who served on the panels and contributed material to the panels are listed in the section following the committee list. My thanks to all of them. I also thank the staff of the National Research Council for their efforts. Frances Walton cheerfully provided the administrative support necessary for the committee to meet and function. Kathy Marshall spent long hours skillfully preparing the many drafts of the manuscript. Caitilin Gordon provided expert editorial assistance. Walt Rosen and David Policansky provided panel support early in the project and continued to contribute as the project progressed. In particular, I acknowledge the dedicated staff support of John Burris and Cliff Gabriel. John was the project director throughout the effort, organizing the committee and helping it through the early drafts. Cliff shepherded the effort through its later stages, assuming oversight of the manuscript in later drafts and the review process, a labor of great effort and dedication. To them, and all others who worked so hard to produce this study, I offer my most sincere appreciation. PETER H. RAVEN, Chairman Committee on Research Opportunities in Biology

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Contents EXECUTIVE SUMMARY 1 THE NEW BIOLOGY 2 NEW TECHNOLOGIES AND INSTRUMENTATION RECOMBINANT DNA TECHNIQUES, 19 Transformation of Higher Organisms, 21; Making a Transgenic Animal, 23; Creating Transgenic Plants, 26; Future Prospects, 26 MONOCLONAL ANIIBODES, 27 MICROCHEMICAL TECHNIQUES, 28 FLOW CYTOMETRY, 31 MICROSCOPY, 32 Video-Enhanced Contrast Microscopy, 33; Low-Light-Dose Microscopy, 33; Scanning Acoustic Microscope, 34; Scanning Tunneling and Atomic Force Microscope, 34 MAGNETIC RESONANCE, 35 COMPUTERS AND DATA ANALYSIS, 36 BIOLOGY AND THE FUTURE, 37 15 19 3 MOLECULAR STRUCTURE AND FUNCTION 39 PRIMARY STRUCTURE, 43 THREE-DIMENSIONAL STRUCTURE, 51 MOLECULAR ASSEMBLES, 60 DIRECTED MODIFICATION OF PROTEINS, 67 FOLDING, 71 NEW TECHNIQUES AND INSTRUMENTATION, 75 . . ~ Ill

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All 4 GENES AND CELLS ........................ RESEARCH STRATEGIES, 78 THE NUCLEUS, 79 Nuclear Envelope, 80; Chromosomes, 81; The Nucleolus, 84 GENES AND GENE ACTION, 84 Genetic Analysis, 85; The Genome, 88; DNA Replication, 90; Recombination, 93; DNA Repair and Mutagenesis, 96; Gene Expression, 98; Genome Organization, 103 CYTOPLASM: ORGANELLES AND FUNCTIONS, 104 Protein Synthesis and Regulation, 105 MITOCHONDRIA: FUNCTION AND BIOGENESIS, 108 CELL MOTILITY AND THE CYTOSKELETON, 111 Cell Structure, 111; Cell Movement, 113 CELL MEMBRANE, 115 THE EXTRACELLULAR MATRIX OF ANIMALS, 117 CELL REGULATION, 118 Cell Division, 118; Cell-to-Cell Communication, 120; Growth Factors, 122; Receptors, 123; Transmembrane Signaling, 124; Oncogenes, 133 GENERAL PLANT CELL BIOLOGY, 134 Chloroplasts, 135; The Plant Cell Wall, 137 5 DEVEL()PMENT COlVTENTS 77 .......... 140 DEVELOPMENT BEGINS WITH GAMETOGENESIS, 142 CELL DIVISION, GROWTH, AND DEVELOPMENTAL TIMING, 146 DlFFiiRENTL\L GENE EXPRESSION, 153 CELL MOVEMENT AND CELL ADHESION, 159 POSITIONAL INFORMATION, 164 DEVELOPMENT IS FOR ADULT ANIMALS TOO, 167 SPECIAL PROBLEMS IN PLANT DEVELOPMENT, 169 Plant Cell Growth, 171; The Development of Plant Organs, 174 6 THE NERVOUS SYSTEM AND BEHAVIOR .... NERVE CELL COMMUNICATION, 182 THE CYTOSKELETON AND TO TRANSPORT OF MATERIALS WITH NERVE CELLS, 187 Slow Axonal Transport, 188; Rapid Axonal Transport, 189 DEVELOPMENT OF THE NERVOUS SYSTEM, 189 Selective Cell Aggregation, 192 NEURAL PLASTICITY AND ELEMENTARY FORMS OF LEARNING, 198 175

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CONTENTS NEUROBIOLOGY OF PERCEPTION: VISION, 201 Behavioral Studies of Vision in Animals, 204 NEUROBIOLOGY OF MOTOR CONTROL, 205 NEUROBIOLOGY OF COGNITION, 210 Attention, 212; Psychobiology of Development, 213 BEHAVIORAL ECOLOGY, 214 ABNORMALITIES OF BEHAVIOR, 219 7 THE IMMUNE SYSTEM AND INFECTIOUS DISEASES . e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e THE IMMUNE SYSTEM, 224 Specificity of the Immune Response, 225; B Lymphocytes, 229; T Cells, 233; Regulation of the Immune Response, 239; Complement and Other Effector Molecules, 241; Hypersensitivity, Inflammation, and Phagocytosis, 241 INFECTIOUS DISEASES, 244 Entry into the Host, 245; Spread in the Host, 249; Interactions of Kineses with the Host Cell, 251; Cell and Tissue Tropism, 252; How Is Injury Mediated?, 254; Persistent Infections, 258 CONCLUSION, 258 xv -224 8 EVOLUTION AND DIVERSITY 260 THE EVOLUTIONARY PROCESS, 265 THE RESULT OF EVOLUTION, 270 EVOLUTIONARY HISTORY, 279 CURRENT STATUS OF RESEARCH, 283 Collections and Special Facilities, 284 9 ECOLOGY AND ECOSYSTEMS 287 INTRODUCTION, 287 IDEAS AND APPROACHES IN ECOLOGY, 288 The Responses of Organisms to Environmental Variations, 288; Structure and Regulation of Populations, 290; Chemical Ecology, 292; Behavioral Ecology, 295; Genetic Ecology, 298; The Union of Behavioral, Population, and Genetic Ecology, 299; Ecosystem and Community Ecology, 301 HUMAN-CAUSED ENVIRONMENTAL CHANGES, THE PROBLEMS THEY CAUSE, AND SOME SOLUTIONS, 305 Species Loss and Conservation Ecology, 307; Global Climate Change, 313 TECHNOLOGICAL AND METHODOLOGICAL ADVANCES, 314

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XVI i Remote Sensing, 314; Analytic Chemistry, 315; Tools for Studying Paleoecology, 315; Stable Isotopes, 316; Biotechnology, 317; Models in Ecology, 317 CONCLUSION, 321 10 ADVANCES IN MEDICINE,- THE BIOCHEMICAL PROCESS INDUSTRY, AND ANIMAL AGRICULTURE . e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e e ADVANCES IN MEDICINE, 323 Molecular Pharmacology and Human Disease, 324; New Approaches to Understanding Health and Disease: The Lipoproteins, 328 ARTHRITIS, 334 CANCER: CURRENT STATUS AND SOME NEW APPROACHES TO ITS CONTROL, 336 Cancer Therapy, 337; Newer Approaches to Cancer Control, 339 ADVANCES IN UNDERSTANDING HUMAN GENETIC DISORDERS, 344 Elucidation of the Primary Genetic Defect, 345; Gene Diagnosis, 346; Gene Therapy, 347 NEW APPROACHES FOR CONTROL OF MICROBIAL INFECTION, 348 Vaccines, 349; Antiviral Agents, 351 ADVANCES IN THE BIOCHEMICAL PROCESS INDUSTRY, 352 Goals in Industrial Biotechnology, 353 ADVANCES IN ANIMAL AGRICULTURE, 359 Growth Regulation, 360; Reproduction, 361; Lactation, 362; Infectious Disease, 362; Production of Feedstocks, 363; Livestock Improvement, 363 11 PLANT BIOLOGY AND AGRICULTURE............... PLANTS AND THEIR ENVIRONMENT, 366 PHOTOSYNTHESIS, 371 NITROGEN FIXATION, 377 PLANT GROWTH AND DEVELOPMENT, 381 Plant Hormones, 381; Environment, 384; Plant Reproduction, 385 PLANT-PATHOGEN INTERACTIONS, 390 GENETIC IMPROVEMENT OF PLANTS, 397 Tissue Culture, 397; Plant Cell Transformation, 400 CONTENTS 323 365

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CONTENTS 12 BIOLOGY RESEARCH INFRASTRUCTURE AND RECOMMENDATIONS .............................. TRAINING, 405 Women and Minondes, 409; Current Training Needs, 409 EMPLOYMENT, 412 LABORATORY COSTS AND EQUIPMENT NEEDS, 414 FUNDING, 416 LARGE DATA BASES AND REPOSITORIES, 420 RESEARCH CENTERS AND THE INDIVIDUAL INVESTIGATOR, 421 REFERENCES AND NOTES, 422 INDEX XVt! 403 425

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OPPORTUNITIES IN BIOLOGY -

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