The Dynamic Genome: Barbara McClintock's Ideas in the Century of Genetics

Edited by Nina Fedoroff, Carnegie Institution of Washington, and David I Botstein, Stanford University School of Medicine Barbara McClintock was born in 1902, within a few years of the rediscovery of Mendel's laws. Her life, discoveries, and insights span the history of genetics in this century. ! In the 1920s, she became a dominant figure in the group that flourished at Cornell University under R.A. Emerson and made remarkable technical and conceptual advances in maize cytogenetics. These studies continued at the California Institute of Technology, in Freiburg, Germany, and at the University of Missouri. In 1942, she joined the staff of the Carnegie Institution of Washington at Cold Spring Harbor, New York, where she remains a Distinguished Service Member. McClintock's unique ability to discern relationships between the behavior of chromosomes and the properties of the whole organism earned her early recognition. She was elected to the National Academy of Sciences in 1944 and to the presidency of the Genetics Society of America in 1945. Had she done no more, McClintock would have become a major figure in the history of genetics. But at Cold Spring Harbor, she began the studies of the consequence of dicentric chromosome formation and breakage that led her to the discovery of genetic elements capable of moving within the genome and controlling expression of other genes. Although McClintock was universally respected and admired, the first reaction to these findings was often uncomprehending or indiferent, even dismissive. In due course, however, the generality of mobile genetic elements and the concept of a dynamic genome were understood and widely accepted, culminating in the award to McClintock of an unshared Nobel Prize in 1983. As Barbara's 90th birthday approached, some of her many friends and colleagues were invited to write essays for the occasion. This book contains a kaleidoscope of contributions, many by those who discovered transposition in other organisms. Their essays give a remarkable account of the scientific legacy of one of the century's greatest geneticists. CONTENTS Introduction (N. Fedoroff, D. Botstein) Transposable Elements: Tire Collected Papers of Barbara McClintock. Cytogenetics Kernels and Colonies: The Challenge of Pattern (J.A. Shapiro); Phage Reprint of Creighton and McCiintock 1931. A Correlation of Mu: An Early Prokaryotic Controlling Element (M.M. Howe); Cytological attd Genetical Crossing-over in Zea mays. Recollections Discovery of the Bacterial Transposon TnlO (D. Botstein); McClintock of Barbara McClintock's Cornell Years (H.B. Creighton); Barbara (1933): Implications for Meiotic Chromosome Pairing (N. Kleckner); McClintock: Reminiscences (C. Burnham); Barbara McClintock: Twenty-five Years of Transposable Element Research in K61n (H Recollections of a Graduate Student (H.V. Crouse); Neurospora Saedler, P. Starlinger); Obsession with Sequences (N.D.F. Grindley); Chromosomes (D.D. Perkins); The Early Years of Maize Genetics The Revenge of the Mayans (G. Albrecht-Buehler); "Please Come to (M.M. Rhoades) My Laboratory for Better Coffee, Fresh Orange Juice . . . Transposition Conversation" (B.M. Alberts); Transposable Elements (Ty) in Yeast Reprint of McClintock 1952. Chromosome Organization and Genic (G.R. Fink); Controlling Elements, Mutable Alleles, and Mating-type Expression. Insertion by Phages and Transposons (A. Campbell); Cold Interconversion (I. Herskowitz); Thinking about Programmed Genome Spring Harbor 1944 1955: A Minimemoir (E.M. Witkin); Annals of Rearrangements in a Genome Static State of Mind (J.N. Strathern); Mobile DNA Elements in Drosophila: The Impact and Influence of The Role of McClintock's Controlling Element Concept in the Story of Barbara McCiintock (M. Green); The Mutable waxy and bronzel Yeast Mating-type Switching (A.J.S. Klar); From Bacterial Flagella to Alleles of Maize (O.E. Nelson); Remembrances of Barbara Homeodomains (M.I. Simon); Discovery of Tcl in the Nematode, McClintock (O.L. Miller, Jr.); The Nucleolar-organizing Element (J.G. Caenorhabditis elegans (P. Anderson et ai.); Reprint of McClintock Gall); Do Some "Parasitic" DNA Elements Earn an Honest Living? 1978. Mechanisms That Rapidly Reorganize the Genome (M.-L. Pardue); The Plural of Heterochromatin (C.D. Laird); A The Nobel Prize and a Molecular Retrospective Tapestry of Transposition (A.M. Skalka); Reprint of McCiintock 1956. Reprint of McClintock 1984. Nobel Prize Lecture: The Significance of hrtranuclear Systems Controlling Gene Action and Mutation Responses of the Genome to Challenge. Broken Chromosomes and Retirement Telomeres (E.H. Blackburn); Maize Transposable Elements: A Story Reprint of Introduction. The Discovety and Characterization of in Four Parts (N.V. Fedoroff) 1992, 422 pp., illus, indexes ISBN 0-87969-422-X Cloth $65

Reader Service No. 795 GENES

DEVELOPMENT

VOLUME 6 NUMBER 8 PAGES 1357-1588 AUGUST 1992

EDITORIAL BOARD J. Adams (Melbourne, Australia) P. Ingham (Oxford, UK) Editors M. Ashburner (Cambridge, UK) N. Jones (London, UK) T. Grodzicker (Cold Spring Harbor) J. Beckwith (Boston, USA} R. Losick (Cambridge, USA) N. Hastie (Edinburgh) T. Cech (Boulder, USA) J. Manley (New York, USA) P. Chambon (Strasbourg, France) D. McClay (Durham, USA) Managing Editor N.-H. Chua (New York, USA) W. McGinnis (New Haven, USA) J. Cuddihy (Cold Spring Harbor) E. Coen (Norwich, UK) S. McKnight (Baltimore, USA) J. Coffin (Boston, USA) A. McMahon (Nutley, USA) S. Courtneidge (Heidelberg, FRG) P. Nurse (Oxford, UK) E. De Robertis (Los Angeles, USA) C. Niisslein-Volhard (Tubingen, FRG) R. Evans (La Jolla, USA) R. Palmiter (Seattle, USA) G. Fink (Cambridge, USA) G. Rubin (Berkeley, USA) P. Goodfellow (London, UK) U. Schibler (Geneva, Switzerland) S. Gottesman (Bethesda, USA) M. Scott {Stanford, USA) T. Graf (Heidelberg, FRG) D. Solter (Freiburg, FRG) C. Gross (Madison, USA) J. Steitz (New Haven, USA) F. Grosveld (London, UK) J. Strathern (Frederick, USA) M. Groudine (Seattle, USA) T. Taniguchi (Osaka, Japan) L. Guarente (Cambridge, USA) S. Tilghman (Princeton, USA) C. Guthrie (San Francisco, USA) R. Tjian (Berkeley, USA) W. Herr (Cold Spring Harbor, USA) H. Varmus (San Francisco, USA) J. Hodgkin (Cambridge, UK) E. Wagner (Vienna, Austria) B. Hogan (Nashville, USA) V. Walbot (Stanford, USA) R. Horvitz (Cambridge, USA) M. Wigler (Cold Spring Harbor, USA)

EDITORIAL OFFICES Editorial~Production United States United Kingdom N. Dumser, Technical Editor Cold Spring Harbor Laboratory Press MRC Human Genetics Unit C. Kuret, Production Editor Box i00, 1 Bungtown Road Western General Hospital L. Hearfield, Editorial Secretary Cold Spring Harbor, New York 11724-2203 Crewe Road Phone 516-367-8492 Edinburgh EH4 2XU, UK FAX 516-367-8532 Phone 031-332-8676 FAX 031-332-7359

GENES & DEVELOPMENT (ISSN 0890-9369 is published monthly for $360 M. Merrick, Treasurer, Genetical Society, AFRC Unit of Nitrogen Fixa- (institutional), $105 {individual making personal payment), $138 (Gene- tion, University of Sussex, Falmer, Brighton, Sussex BN1 9RH; tele- tical Society of Great Britain members) by Cold Spring Harbor Labora- phone 011-44-606755 ext 8240; FAX 011-44-273-678133. tory Press, Bungtown Road, Cold Spring Harbor, New York 11724, in Claims for missing issues must be received within 4 months of issue association with the Genetical Society of Great Britain. Second-class date. postage is paid at Cold Spring Harbor and additional mailing offices. Change of address Please enclose recent mailing label with address POSTMASTER: Send address changes to Cold Spring Harbor Laboratory Press, POB 100, 1 Bungtown Rd., Cold Spring Harbor, New York 11724- change; allow 4 weeks. 2203. Advertising To advertise in Genes & Development, contact Nancy Subscription Price Orders may be sent to Cold Spring Harbor Labora- Kuhle, Advertising Managei, Cold Spring Harbor Laboratory Press, Cold tory Press, Fulfillment Department, 10 Skyline Drive, Plainview, NY Spring Harbor, New York 11724-2203; telephone 516-367-8351. 11803-9729. Telephone: Continental US except NY State, 1-800-843- Photo Copy Authorization to photocopy items for internal or personal 4388; all other locations, 516-394-1930/1931/1932. FAX 516-349-1946. use, or the internal or personal use of specific clients, is granted by Cold Volume 6, 1992, $360, U.S. institutional; $435, R.O.W. institutional. Spring Harbor Laboratory Press for libraries and other users registered Personal subscription rate: $105, U.S.; $180, R.O.W. Price includes sur- with the Copyright Clearance Center (CCC} Transactional Reporting face postage for U.S. and airlift for R.O.W. Genetical Society members, Service, provided that the base fee of $3.00 per copy is paid directly to $138.00. All subscriptions are entered for the calendar year and must be CCC, 21 Congress St., Salem, MA 01970 (0890-9369/92 $3.00 + 0.). This prepaid. Personal subscriptions must be prepaid by personal check, consent does not extend to other kinds of copying, such as copying for credit card, or money order. All checks must be for US dollars and drawn general distribution for advertising or promotional purposes, for creating on a US bank. Genetical Society members may also subscribe by check, new collective works, or for resale. payable to the Genetical Society, for £80 (includes airlift). Send to: Dr. Copyright © 1992 by Cold Spring Harbor Laboratory Press GENES & DEVELOPMENT August 1992 Contents

Research papers A tyrosyl-tRNA synthetase binds specifically to the group I intron catalytic core 1357 Qingbin Guo and Alan M. Lambowitz

Activation of the catalytic core of a group I intron by a remote 3' splice junction 1373 Frangois Michel, Luc Jaeger, Eric Westhof, Richard Kuras, Fr6d6rique Tihy, Ming-Qun Xu, and David A. Shub

The mechanism of somatic inhibition of Drosophila P-element pre-mRNA splicing: 1386 multiprotein complexes at an exon pseudo-5' splice site control U1 snRNP binding Christian W. Siebel, Lucille D. Fresco, and Donald C. Rio

The consequences of expressing hsp70 in Drosophila cells at normal temperatures 1402 Juliana H. Feder, Janice M. Rossi, Jonathan Solomon, Noah Solomon, and Susan Lindquist

CIKI: a developmentally regulated spindle pole body-associated protein important for 1414 microtubule functions in Saccharomyces cerevisiae Barbara D. Page and Michael Snyder

Deficiency of an enzyme of tyrosine metabolism underlies altered gene expression in newborn 1430 liver of lethal albino mice Siegfried Ruppert, Gavin Kelsey, Andreas Schedl, Erika Schmid, Edda Thies, and Gfnther Schftz

Cachexia and graft-vs.-host-disease-type skin changes in keratin promoter-driven TNFa 1444 transgenic mice Jian Cheng, Kursad Turksen, Qian-Chun Yu, Hans Schreiber, Michael Teng, and Elaine Fuchs

Endogenous retroviral sequences are required for tissue-specific expression of a human salivary 1457 amylase gene Chao-Nan Ting, Michael P. Rosenberg, Claudette M. Snow, Linda C. Samuelson, and Miriam H. Meisler

Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of 1466 Id with E2A proteins Yale Jen, Harold Weintraub, and Robert Benezra

Myc family oncoproteins function through a common pathway to transform normal cells in 1480 culture: cross-interference by Max and trans-acting dominant mutants Bhaskar Mukherjee, Sharon D. Morgenbesser, and Ronald A. DePinho

The cell-type-specific activator region of c-Jun juxtaposes constitutive and negatively 1493 regulated domains Vijay R. Baichwal, Adam Park, and Robert Tjian The Drosophila spitz gene encodes a putative EGF-like growth factor involved in 1503 dorsal-ventral axis formation and neurogenesis Barbara J. Rutledge, Kang Zhang, Ethan Bier, Yuh Nung Jan, and Norbert Perrimon dorsal-twist interactions establish snail expression in the presumptive mesoderm of the 1518 Drosophila embryo Y. Tony Ip, Ronald E. Park, David Kosman, Karina Yazdanbakhsh, and Michael Levine zeste, a nonessential gene, potently activates Ultrabithorax transcription in the 1531 Drosophila embryo Jeffrey D. Laney and Mark D. Biggin

Functional analysis of Drosophila transcription factor IIB 1542 Sharon L. Wampler and James T. Kadonaga

The basis for the mechanistic bias for deletional over inversional V(D)J recombination 1553 George H. Gauss and Michael R. Lieber

A protein-binding site in the c-myc promoter functions as a terminator of RNA polymerase 1562 II transcription Sadia Roberts, Tracey Purton, and David L. Bentley

Transition from rapid processive to slow nonprocessive polyadenylation by vaccinia virus 1575 poly(A) polymerase catalytic subunit is regulated by the net length of the poly(A) tail Paul David Gershon and Bernard Moss

Product news 1587

Cover In situ hybridizationof fumarytacetoacetate hydrolase cDNA probe to sections of day-17.5 fetal mouse kidney. (For details, see Ruppert et al., p. 1430.)