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Methods in Cell Biology
VOLUME 106
Caenorhabditis elegans: Molecular Genetics and Development
2nd Edition
Series Editors
Leslie Wilson
Department of Molecular, Cellular and Developmental Biology
University of California
Santa Barbara, California

Paul Matsudaira
Department of Biological Sciences
National University of Singapore
Singapore
Methods in Cell Biology

VOLUME 106
Caenorhabditis elegans: Molecular Genetics and Development
2nd Edition

Edited by
Joel H. Rothman
Professor and Chair, Department of MCD Biology,
University of California, Santa Barbara, CA, USA

Andrew Singson
Associate Professor, Rutgers University,
Waksman Institute, Piscataway, NJ, USA

AMSTERDAM  BOSTON  HEIDELBERG  LONDON

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CONTRIBUTORS

Numbers in parentheses indicate the pages on which the author’s contributions

begin.

Shirin Bahmanyar (289), Ludwig Institute for Cancer Research and Department of
Cellular & Molecular Medicine, University of California San Diego, La Jolla,
California, USA
Jean-Louis Bessereau (65), Ecole Normale Sup erieure, Institut de Biologie de
l’ENS, IBENS, Paris, France; INSERM U1024, Paris, France; CNRS, UMR
8197, Paris, France
Thomas Blumenthal (187), Department of Molecular, Cellular, and Developmental
Biology, University of Colorado, Boulder, Colorado, USA
Gina Broitman-Maduro (253), Department of Biology, University of California at
Riverside, Riverside, California, USA
Ana Carvalho (289), Ludwig Institute for Cancer Research and Department of
Cellular & Molecular Medicine, University of California San Diego, La Jolla,
California, USA
Shih-Peng Chan (219), Department of Molecular, Cellular and Developmental
Biology, Yale University, New Haven, Connecticut, USA; Current address:
Department of Microbiology, College of Medicine, National Taiwan University,
Taipei, Taiwan
Iain Cheeseman (289), Whitehead Institute for Biomedical Research, MIT,
Cambridge, MA, USA
Andrew D. Chisholm (325), Section of Cell and Developmental Biology, Division
of Biological Sciences, University of California, San Diego, La Jolla, California,
USA
Patricia G. Cipriani (89), Center for Genomics and Systems Biology; Department
of Biology, New York University, New York, NY 10003
Arshad Desai (289), Ludwig Institute for Cancer Research and Department of
Cellular & Molecular Medicine, University of California San Diego, La Jolla,
California, USA
Julien Dumont (289), Institut Curie-UMR144, Paris, France
Brian D. Geldziler (343), Waksman Institute, Rutgers University, Department of
Microbiology and Molecular Genetics, Piscataway, New Jersey, USA
Claudiu A. Giurumescu (325), Section of Cell and Developmental Biology,
Division of Biological Sciences, University of California, San Diego, La Jolla,
California, USA

xi
xii Contributors

Reto Gassmann (289), Ludwig Institute for Cancer Research and Department of
Cellular & Molecular Medicine, University of California San Diego, La Jolla,
California, USA
Jeff Hardin (377), Department of Zoology, University of Wisconsin-Madison,
Madison, Wisconsin, USA
Pan-Young Jeong (445), Present address: Department of Molecular, Cellular and
Developmental Biology, University of California Santa Barbara, Santa Barbara,
California, USA
Yishi Jin (413), Howard Hughes Medical Institute, Neurobiology Section, Division
of Biological Sciences, University of California, San Diego, La Jolla, California,
USA
Martin R. Jones (23), Department of Medical Genetics, University of British
Columbia, Vancouver, British Columbia, Canada
Hyoe-Jin Joo (445), Yonsei Proteome Research Center, Department of
Biochemistry and Biomedical Science, College of Life Science and
Biotechnology, World Class University Program, Graduate School, Yonsei
University, Seoul, Korea
Heekyeong Kim (445), Yonsei Proteome Research Center, Department of
Biochemistry and Biomedical Science, College of Life Science and
Biotechnology, World Class University Program, Graduate School, Yonsei
University, Seoul, Korea
Kwang-Youl Kim (445), Yonsei Proteome Research Center, Department of
Biochemistry and Biomedical Science, College of Life Science and
Biotechnology, World Class University Program, Graduate School, Yonsei
University, Seoul, Korea
Eric J. Lambie (3), Biology Department II, Ludwig-Maximilians-University,
Munich, Germany
Jeeyong Lee (445), Yonsei Proteome Research Center, Department of Biochemistry
and Biomedical Science, College of Life Science and Biotechnology, World Class
University Program, Graduate School, Yonsei University, Seoul, Korea
Zoe Lohn (23), Department of Medical Genetics, University of British Columbia,
Vancouver, British Columbia, Canada
Paul Maddox (289), Institute for Research in Immunology and Cancer, Department
of Pathology and Cell Biology, University of Montreal, Montreal, Quebec, Canada
Morris F. Maduro (161, 253), Department of Biology, University of California
Riverside, Riverside, California, USA
Matthew R. Marcello (343), Waksman Institute, Rutgers University, Department of
Microbiology and Molecular Genetics, Piscataway, New Jersey, USA; UMDNJ-
Robert Wood Johnson Medical School, Piscataway, New Jersey, USA
J. Jason Morton (187), Department of Molecular, Cellular, and Developmental
Biology, University of Colorado, Boulder, Colorado, USA
Sherry Niessen (289), The Skaggs Institute for Chemical Biology and Department
of Chemical Physiology, The Center for Physiological Proteomics, The Scripps
Research Institute, La Jolla, California, USA
Contributors xiii

Karen Oegema (289), Ludwig Institute for Cancer Research and Department of
Cellular & Molecular Medicine, University of California San Diego, La Jolla,
California, USA
Young-Ki Paik (445), Yonsei Proteome Research Center, Department of
Biochemistry and Biomedical Science, College of Life Science and
Biotechnology, World Class University Program, Graduate School, Yonsei
University, Seoul, Korea; Rm#423, Industry-University Research Bldg., Yonsei
University, 134, Shinchon-dong, Sudaemoon-ku, Seoul, Korea
Amy E. Pasquinelli (219), Department of Biology, University of California San
Diego, La Jolla, California, USA
Fabio Piano (89), Center for Genomics and Systems Biology; Department of
Biology, New York University, New York, NY 10003; New York University
Abu Dhabi, Abu Dhabi, United Arab Emirates
Vida Praitis (161), Biology Department, Grinnell College, Grinnell, Iowa, USA
erie J.P. Robert (65), Ecole Normale Sup
Val erieure, Institut de Biologie de l’ENS,
IBENS, Paris, France; INSERM U1024, Paris, France; CNRS, UMR 8197, Paris,
France; Present address: Laboratory of Molecular and Cellular Biology,
UMR5239 CNRS, Ecole Normale Sup erieure de Lyon, Lyon, France
Ann M. Rose (23), Department of Medical Genetics, University of British
Columbia, Vancouver, British Columbia, Canada
Diane C. Shakes (343), College of William and Mary, Department of Biology,
Williamsburg, Virginia, USA
Andrew Singson (343), Waksman Institute, Rutgers University, Department of
Microbiology and Molecular Genetics, Piscataway, New Jersey, USA
David R. Sherwood (113), Department of Biology, Duke University, Durham, North
Carolina, USA
Frank J. Slack (219), Department of Molecular, Cellular and Developmental
Biology, Yale University, New Haven, Connecticut, USA
Albertha J.M. Walhout (271), Program in Gene Function and Expression and
Program in Molecular Medicine, University of Massachusetts Medical School,
USA
Zheng Wang (113), Department of Biology, Duke University, Durham, North
Carolina, USA
Priscilla M. Van Wynsberghe (219), Department of Biology, University of
California San Diego, La Jolla, California, USA; Current address: Department
of Biology, Colgate University, Hamilton, NY, USA
Dong Yan (413), Howard Hughes Medical Institute, Neurobiology Section, Division
of Biological Sciences, University of California, San Diego, La Jolla, California,
USA
John R. Yates III (289), The Skaggs Institute for Chemical Biology and Department
of Chemical Physiology, The Center for Physiological Proteomics, The Scripps
Research Institute, La Jolla, California, USA
Esther Zanin (289), Ludwig Institute for Cancer Research and Department of
Cellular & Molecular Medicine, University of California San Diego, La Jolla,
California, USA
PREFACE

Caenorhabditis elegans: Molecular Genetics and Development

The allure of a model organism comes not from any special fascination for the
creature itself; it is doubtful that most researchers studying a simple and tiny animal,
the nematode Caenorhabditis elegans, are particularly attracted to these modest
creatures per se. Rather than any fondness for the animal, it is the exceptional
experimental methodology available with these high-performance vehicles of bio-
logical discovery that entice those driven by intellectual curiosity about the living
world to investigate their inner workings. As this millimeter-long creature has amply
proven itself to be of enduring utility for biological discovery, it is of value to
continue to assemble and update experimental methodology on its use.
A century, in fact a millennium, has turned since the last C. elegans volume was
published in the Methods in Cell Biology series (as volume 48). That volume,
‘‘Caenorhabditis elegans: Modern Biological Analysis of an Organism,’’ was the
first major compendium of C. elegans methods and only the second complete
published volume on this creature. Since that volume appeared, several other collec-
tions of methods have been published, notably a brief practical volume edited by I.
Hope, a methods section edited by V. Ambros as a component of the online resource,
Wormbook, and a published volume edited by K. Strange. Nonetheless, for over a
decade and half the original C. elegans methods volume has served as an invaluable
resource to both seasoned and new researchers who focus their scientific curiosity on
C. elegans.
One might reasonably ask, in an era in which printed material is rapidly dissipat-
ing into cyberspace and vast information resources are available online, why a
printed volume is of value. In our view, the accessibility of a printed form is still
well-suited to the laboratory environment. Several copies of the 1995 C. elegans
methods volume are stationed at ready access on our laboratory shelves. Members of
our laboratories continually reach for the book, even many years after its publication.
Just as laboratory notebooks have yet to be satisfactorily replaced by a digital
medium, the ability to flip through the pages of a methods volume is not yet an
anachronism in the setting of an experimental laboratory.
We are closing in on the 50th anniversary of Sydney Brenner’s 1963 letter to the
director of the Medical Research Council Laboratory of Molecular Biology, immor-
talized in the first Cold Spring Harbor Press C. elegans monograph, in which he
proposed to adopt a Caenorhabditis worm as a model organism. The period since the
predecessor of this volume was published in 1995 is a fraction of that interval and yet
has seen the majority of the prominent discoveries made with the animal. Six Nobel
laureates in the C. elegans community have been celebrated since the last volume in

xv
xvi Preface

this series was published and key discoveries that led to some of those prizes were
made during this period. This era also saw the first complete animal genome
sequence, the discovery of RNAi, the generality of miRNA-mediated control across
biology, and many other fundamental advances that have emerged from the labora-
tories of C. elegans investigators and have proven to be broadly transformative to
biology.While advances made with the worm are quantifiable, their full impact on
science is inestimable.
The original volume made an effort to be fully comprehensive. In earlier days, it
was possible to craft a single volume that fully addressed the state of the art. But the
precipitous growth in the field would make such an undertaking unwieldy, if not
impractical. 85% of all publications in the Pubmed database containing the text word
‘‘elegans’’ (currently approximately 20,000) were published since the last volume
appeared, many by labs that have not traditionally focused on the animal. The
number of C. elegans laboratories with strain designations (now over 850) is more
than five times that in 1995. A compendium of methods that scaled similarly might
contain over 170 chapters spread over as many as 10 volumes. Thus, the two volumes
assembled here no longer attempt to serve as a single source book for C. elegans
methodology. Rather, we have chosen to include chapters on many of the methods
that have evolved or dramatically altered since the 1995 volume, with the recognition
that more has been left out than included. It is inevitable that additional volumes will
come in the future that fill and update voids left by the current collection.
Owing to the length of this updated collection, it is now distributed over two
volumes. This volume (vol. 106 in the series) comprises genetics, molecular biology,
and development, while the subsequent volume (vol. 107) will focus on imaging, cell
biology, and physiology. Many methods from the original 1995 volume (e.g., basic
culturing, mutagenesis, mosaic analysis, and so on) are still relevant and useful and
the experimentalist is encouraged to consult that volume for such methods. It is
inevitable that some of the methods in the earlier volume (e.g., the physical map,
genomic and cDNA sequencing, and use of the extinct database structures that
preceded Wormbase) have become obsolete. On the other hand, many methods have
been improved or refined for specific applications, for example, genetic mapping
techniques (Chapter 1), reverse genetic approaches (Chapters 3 and 4), transgenesis
(Chapter 6), and in situ hybridization using RNA probes (Chapter 9), all of which are
covered in this volume as revised or entirely new chapters. We note that, unlike the
previous edition, we have not included comprehensive appendices, as this informa-
tion is now readily available in a continually updated manner online through the
internet resources listed in the single Appendix of this volume.
Mastery of the varied tools of C. elegans biology is enhanced by the experience
gained in a lab connected to those that grew up during formative stages of the field.
The lore, philosophy, and strategies one uses to dissect biological processes are not
coherently incorporated in the literature, but can be effectively transmitted through a
sort of apprenticeship in such labs.The worm field is famed for the large fraction of
practitioners who trace lineal roots to the early pioneers in the field. However, over
recent years, the prominence of the worm system has lured many researchers not
Preface xvii

formally linked to the ‘‘worm pedigree’’ to adopt the animal as a useful tool for their
favorite subjects of inquiry. Thus, rather than covering discrete methods per se, some
of the chapters are designed to transmit strategies that are not easily gleaned from the
literature (most prominently featured in Chapter 5, which describes genetic strate-
gies used to deconstruct the pathways that drive cellular and developmental pro-
cesses, and also in the chapters on mapping and on specialized chromosomes in
Chapters 1 and 2.) We believe that these strategies will be of particular value to
newcomers who learn worm biology without the benefits of apprenticeship in a
seasoned worm lab.
Among the most notable of the advances in C. elegans technology since the first
volume was published was the discovery of RNAi and subsequent methods for
adapting RNAi to broad functional genomics screens, which have revolutionized
discovery of gene function. Such approaches, and the integration of the ‘‘phenome’’
with informatics studies of functional relationships between gene activities, are
covered in chapter 4, of value to aficionados and newcomers alike. Similarly, the
recognition that miRNAs function at many levels across animal biology make
chapter 8, on analysis of miRNAs, an essential component of this volume. In
addition, since publication of the earlier volume, it has become clear that a large
fraction of worms genes are organized in operons and are trans-spliced. Any worm
molecular geneticist must be mindful of this complexity of gene organization in the
animal and the methods for analyzing RNA processing (Chapter 7) are therefore
important to any researcher considering the structure of genes and effects of muta-
tions and RNAi on gene expression.
An overarching goal articulated by Sydney Brenner when he inaugurated
C. elegans research was to obtain a complete description of the animal: this began
with the comprehensive analysis of the cell lineage and anatomy and later the whole
genome. More recently, this goal has been extended to the level of gene function and
interaction by techniques covered in chapters that describe functional and transcrip-
tional network analysis (Chapters 4 and 10). Genetic approaches have dominated
C. elegans research; however, biochemical methods have become increasingly more
significant, particularly as the pathway from in vitro discovery to in vivo validation
has shortened, and methods for analyzing protein complexes and other proteomics
approaches are covered in Chapters 11 and 16. The pre-eminent focus of Brenner’s
original vision to exploit C. elegans as a new model system was directed at unveiling
the processes that drive development, the biological challenge that drew many
researchers to the worm. In keeping with the predominance of this discipline, a
major subdivision of this volume comprises five chapters (Chapters 12–16) that
address varied approaches to problems in developmental biology, ranging from cell
lineage analysis (including new advances in automated lineage analysis), fertiliza-
tion, morphogenesis, nervous system development and regulation of the alternative
developmental stage, the dauer larva.
Just as C. elegans develops rapidly, so do technological approaches to analyzing
its biology. It is clear that we are able here to capture only an instant in this rapidly
moving field, and methods have advanced even during the period in which these
xviii Preface

chapters were being assembled and edited. For example, the tremendous advances in
DNA sequencing technology is making whole-genome sequence identification of
mutations inexpensive and routine, thereby superseding much of the traditional
genetic mapping approaches. Moreover, effective new methods for generating geno-
mic modifications based on synthetic nucleases have recently appeared, but came
too late to include in the initial release of this volume.These and untold other
technologies will no doubt occupy the pages of future editions in this series, devoted
to this magnificent living tool for biological discovery.
Appreciation for the richness of technology available to C. elegans researchers,
only partially captured in the current volumes, has been expressed in many ways,
even beyond scientific activity. Two of the traditions at the biennial International
C. elegans meeting are the Worm Show, an evening comedy variety show, and the
Worm Art show, in which artistic members of the worm community pay homage to
the animal through visual arts, films, and crafts, including clothing and even cuddly
stuffed toys. Upon further reflection, perhaps those of us who have dedicated so
many years to pursuing the wonderful mysteries of C. elegans, and appreciative of
the many gifts that it has generously yielded, have indeed developed a deep and
abiding fondness for the modest little creature after all.

Joel H. Rothman and Andrew Singson

August, 2011
ACKNOWLEDGMENTS

We would like to thank all of the chapter authors for their contributions and
patience during the editing of this volume. The scientific community will greatly
benefit from their efforts. We would like to thank the following people who critically
reviewed the various chapters: Allison Abbott, Laura Bianchi, David Fey, Tina
Gumienny, Tim Kroft, Matthew Marcello, Kim McKim, Jeremy Nance, Kevin
O’Connell, Sara Olson, Richard Padgett, Gunasekaran Singaravelu, and Gillian
Stanfield. We are also grateful to Stacey Nocciolo and Cari Donnelly for their
assistance in managing the many files associated with this volume.

xix
PART I

Genetics and Functional Genomics

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