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ANNUAL PLANT REVIEWS
VOLUME 36
ANNUAL PLANT REVIEWS
The Moss Physcomitrella patens

Edited by

Celia D. Knight
Centre for Plant Sciences, Faculty of Biological Sciences, University
of Leeds, Leeds, LS2 9JT, UK

Pierre-François Perroud
Department of Biology, CB#1137, One Brookings Drive, Washington
University, St. Louis, MO 63130-4899, USA

and

David J. Cove
Centre for Plant Sciences, Faculty of Biological Sciences, University
of Leeds, Leeds, LS2 9JT, UK, and
Department of Biology, CB#1137, One Brookings Drive, Washington
University, St. Louis, MO 63130-4899, USA

A John Wiley & Sons, Ltd., Publication

This edition first published 2009


C 2009 Blackwell Publishing Ltd

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Blackwell’s publishing programme has been merged with Wiley’s global Scientific, Technical
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Library of Congress Cataloging-in-Publication Data

The moss Physcomitrella patens / edited by Celia Knight, Pierre-François Perroud,

and David Cove.
p. cm. – (Annual plant reviews; v. 36)
Includes bibliographical references and index.
ISBN 978-1-4051-8189-1 (hardback : alk. paper) 1. Physcomitrella patens. 2. Mosses.
3. Biology. I. Knight, Celia. II. Perroud, Pierre-François. III. Cove, David. IV. Series.
QK535.M67 2009
588 .2–dc22
2008044709
A catalogue record for this book is available from the British Library.

Set in 10/12 pt Palatino by Aptara

R
Inc., New Delhi, India
Printed in Singapore

1 2009
Annual Plant Reviews
A series for researchers and postgraduates in the plant sciences. Each volume
in this series focuses on a theme of topical importance and emphasis is placed
on rapid publication.

Editorial Board:
Prof. Jeremy A. Roberts (Editor-in-Chief), Plant Science Division, School of
Biosciences, University of Nottingham, Sutton Bonington Campus,
Loughborough, Leicestershire, LE12 5RD, UK;
Dr David Evans, School of Biological and Molecular Sciences, Oxford
Brookes University, Headington, Oxford, OX3 0BP;
Prof. Hidemasa Imaseki, Obata-Minami 2419, Moriyama-ku, Nagoya 463,
Japan;
Dr Michael T. McManus, Institute of Molecular BioSciences, Massey
University, Palmerston North, New Zealand;
Dr Jocelyn K.C. Rose, Department of Plant Biology, Cornell University,
Ithaca, New York 14853, USA.

Titles in the series:

1. Arabidopsis
Edited by M. Anderson and J.A. Roberts
2. Biochemistry of Plant Secondary Metabolism
Edited by M. Wink
3. Functions of Plant Secondary Metabolites and their Exploitation in
Biotechnology
Edited by M. Wink
4. Molecular Plant Pathology
Edited by M. Dickinson and J. Beynon
5. Vacuolar Compartments
Edited by D.G. Robinson and J.C. Rogers
6. Plant Reproduction
Edited by S.D. O’Neill and J.A. Roberts
7. Protein–Protein Interactions in Plant Biology
Edited by M.T. McManus, W.A. Laing and A.C. Allan
8. The Plant Cell Wall
Edited by J.K.C. Rose
9. The Golgi Apparatus and the Plant Secretory Pathway
Edited by D.G. Robinson
10. The Plant Cytoskeleton in Cell Differentiation and Development
Edited by P.J. Hussey
11. Plant–Pathogen Interactions
Edited by N.J. Talbot
12. Polarity in Plants
Edited by K. Lindsey
13. Plastids
Edited by S.G. Moller
14. Plant Pigments and their Manipulation
Edited by K.M. Davies
15. Membrane Transport in Plants
Edited by M.R. Blatt
16. Intercellular Communication in Plants
Edited by A.J. Fleming
17. Plant Architecture and Its Manipulation
Edited by CGN Turnbull
18. Plasmodesmata
Edited by K.J. Oparka
19. Plant Epigenetics
Edited by P. Meyer
20. Flowering and Its Manipulation
Edited by C. Ainsworth
21. Endogenous Plant Rhythms
Edited by A. Hall and H. McWatters
22. Control of Primary Metabolism in Plants
Edited by W.C. Plaxton and M.T. McManus
23. Biology of the Plant Cuticle
Edited by M. Riederer
24. Plant Hormone Signaling
Edited by P. Hadden and S.G. Thomas
25. Plant Cell Separation and Adhesion
Edited by J.R. Roberts and Z. Gonzalez-Carranza
26. Senescence Processes in Plants
Edited by S. Gan
27. Seed Development, Dormancy and Germination
Edited by K.J. Bradford and H. Nonogaki
28. Plant Proteomics
Edited by C. Finnie
29. Regulation of Transcription in Plants
Edited by K. Grasser
30. Light and Plant Development
Edited by G. Whitelam
31. Plant Mitochondria
Edited by D.C. Logan
32. Cell Cycle Control and Plant Development
Edited by D. Inz’e
33. Intracellular Signaling in Plants
Edited by Z. Yang
34. Molecular Aspects of Plant Disease Resistance
Edited by Jane Parker
35. Plant Systems Biology
Edited by G. Coruzzi and R. Gutiérrez
36. The Moss Physcomitrella patens
Edited by C.D. Knight, P.-F. Perroud and D.J. Cove
CONTENTS

Contributors x
Preface xiii
Glossary xv

1 Putting Physcomitrella patens on the Tree of Life: The Evolution

and Ecology of Mosses 1
Brent D. Mishler and Melvin J. Oliver
1.1 Introduction to Physcomitrella 1
1.2 The position of P. patens on the Tree of Life 2
1.3 Relationships within the mosses 4
1.4 Evolution and ecology of the mosses 6
1.5 General implications for evolutionary processes in mosses 12

2 The Genetic Basis of Natural Variation in Bryophyte Model Systems 16

Stuart F. McDaniel
2.1 Introduction 17
2.2 Genetic variation among bryophyte populations 17
2.3 Mapping genes underlying natural variants 26
2.4 Assigning genes to phenotypes 32

3 Comparative Genomics 42
Stefan A. Rensing, Daniel Lang, and Andreas D. Zimmer
3.1 Introduction 42
3.2 A short history of P. patens genomics 47
3.3 Features of the P. patens nuclear genome 52
3.4 Comparisons with seed plants and algae 60
3.5 Computational resources for P. patens 66
3.6 Conclusions and outlook 67

4 Gene targeting 76
Yasuko Kamisugi and Andrew C. Cuming
4.1 Introduction 76
4.2 Gene targeting in eukaryotes 77
4.3 Gene targeting in P. patens: practical aspects 81
4.4 Targeted gene replacement versus targeted insertion 96
4.5 Mechanisms of gene targeting 98
4.6 Unanswered questions and future prospects 105

vii
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viii
Contents

5 The Small RNAs of Physcomitrella patens: Expression, Function

and Evolution 113
Michael J. Axtell
5.1 Introduction to small RNAs 113
5.2 Classes of small silencing RNAs 114
5.3 Expression of P. patens small RNAs 118
5.4 Biogenesis of P. patens small RNAs: Dicers, Slicers and
other utensils 127
5.5 Targets of P. patens small RNAs 130
5.6 Evolution of plant miRNAs 133
5.7 Conclusions 137

6 Tip Growth in the Moss Physcomitrella patens 143

Magdalena Bezanilla and Pierre-François Perroud
6.1 Introduction 143
6.2 Morphology and structure of a tip cell 144
6.3 Environmental signals affecting polar cell elongation 147
6.4 Cellular structural components involved in polar cell
elongation 149

7 Gametangia Development in the Moss Physcomitrella patens 167

Rumiko Kofuji, Takeshi Yoshimura, Haruko Inoue, Keiko Sakakibara,
Yuji Hiwatashi, Tetsuya Kurata, Tsuyoshi Aoyama, Kunihiko Ueda,
and Mitsuyasu Hasebe
7.1 Introduction 168
7.2 Development of the gametangia 169
7.3 Development of the gametangia after fertilization is
accompanied by growth of the sporophyte 171
7.4 Gene-trap lines with GUS expression in the gametangia 171
7.5 Future prospects 173

8 Chloroplasts 182
Mamoru Sugita and Setsuyuki Aoki
8.1 Chloroplasts of Physcomitrella patens 183
8.2 Plastid DNA 185
8.3 Transcription of plastid genes by two plastid RNA
polymerases PEP and NEP 189
8.4 Rhythmic expression of the plastid Psbd gene 194
8.5 Post-transcriptional regulation in plastids 196
8.6 Plastid transformation 198
8.7 Chloroplast import 199
8.8 Plastid division 200
8.9 Chloroplast movement 202
 Contents
ix

9 Carbon and Energy Metabolism 211

Mattias Thelander, Anders Nilsson, and Hans Ronne
9.1 Introduction 211
9.2 Carbon and energy allocation 213
9.3 Sucrose metabolism and transport 217
9.4 Hexose metabolism and transport 221
9.5 Energy homeostasis and Snf1-related kinases 227
9.6 Conclusions 239
9.7 Technical note on database searches and tree construction 240

10 Hormonal Regulation of Development by Auxin and Cytokinin

in Moss 246
Klaus von Schwartzenberg
10.1 Major plant hormone routes are established in bryophytes 247
10.2 Auxin 249
10.3 Cytokinin 256
10.4 Auxin and cytokinin interaction 269
10.5 Other growth regulating substances 270

11 The Role of Abscisic Acid in Stress Tolerance 282

Sung Hyun Cho, Klaus von Schwartzenberg, and Ralph Quatrano
11.1 Introduction 283
11.2 Tolerance of P. patens to abiotic stresses and the effects
of ABA 286
11.3 Physiological and morphological changes during the
establishment of tolerance 287
11.4 Expression of stress-related genes 288
11.5 Global responses to stress at the transcription level 291
11.6 The ABA-signalling pathway 292
11.7 Conclusions 293

12 Pathogenesis in Mosses 298

Michael Lawton and Hemalatha Saidasan
12.1 Introduction 299
12.2 Recent advances in molecular plant pathology 300
12.3 Experimental advantages of P. patens 304
12.4 Developing a P. patens pathosystem 308
12.5 Responses of P. patens to infection 318
12.6 Selecting P. patens genes for functional studies of disease 321
12.7 Future directions and opportunities 323

Index 339
Color plates (between pages 174 and 175)
CONTRIBUTORS

Setsuyuki Aoki
Graduate School of Information Science, Nagoya University, Nagoya
464-8601, Japan.

Tsuyoshi Aoyama
Department of Basic Biology, Graduate School of Advanced Studies,
Okazaki 444-8585, Japan.

Michael J. Axtell
Department of Biology, Pennsylvania State University, PA 16802-5301, USA.

Magdalena Bezanilla
Department of Biology, University of Massachusetts, Amherst, MA
01003-9297, USA.

Sung Hyun Cho

Department of Biology, Pennsylvania State University, University Park, PA
16802, USA.

David J. Cove
Department of Biology, Washington University in St. Louis, MO 63130-4899,
USA.
Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Andrew C. Cuming
Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Mitsuyasu Hasebe
National Institute for Basic Biology, Okazaki 444-8585, Japan
Department of Basic Biology, Graduate School of Advanced Studies,
Okazaki 444-8585, Japan
Japan Science and Technology Agency, Okazaki 444-8585, Japan.

Yuji Hiwatashi
National Institute for Basic Biology, Okazaki 444-8585, Japan.
Department of Basic Biology, Graduate School of Advanced Studies,
Okazaki 444-8585, Japan.

x
 Contributors
xi

Haruko Inoue
Graduate School of Natural Science and Technology, Kanazawa University,
Kanazawa 920-1192, Japan.

Yasuko Kamisugi
Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Celia D. Knight
Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Rumiko Kofuji
Graduate School of Natural Science and Technology, Kanazawa University,
Kanazawa 920-1192, Japan.

Tetsuya Kurata
Japan Science and Technology Agency, Okazaki 444-8585, Japan.

Daniel Lang
Plant Biotechnology, University of Freiburg, Freiburg D-79104, Germany.

Michael Lawton
Biotechnology Center for Agriculture and the Environment, Rutgers, The
State University of New Jersey, New Brunswick, NJ 08901-8520, USA.

Stuart F. McDaniel
Department of Biology, Washington University in St. Louis, MO 63130-4899,
USA.

Brent D. Mishler
Department of Integrative Biology, University of California Berkeley,
Berkeley, CA 94720-2465 USA.

Anders Nilsson
Department of Medical Biochemistry and Microbiology, Uppsala University,
Uppsala SE-75123, Sweden.

Melvin J. Oliver
Plant Genetics Research Group, USDA-ARS University of Missouri,
Columbia, MO 65211, USA.

Pierre-François Perroud
Department of Biology, Washington University in St. Louis, MO 63130-4899,
USA.
xii
Contributors

Ralph S. Quatrano
Department of Biology, Washington University in St. Louis, MO 63130-4899,
USA.

Stefan A. Rensing
Freiburg Initiative for Systems Biology, University of Freiburg, Freiburg
D-79104, Germany.

Hans Ronne
Department of Medical Biochemistry and Microbiology, Uppsala University,
Uppsala SE-75123, Sweden.

Hemalatha Saidasan
Biotechnology Center for Agriculture and the Environment, Rutgers, The
State University of New Jersey, New Brunswick, NJ 08901-8520, USA.

Keiko Sakakibara
School of Biological Sciences, Monash University, Melbourne, Victoria 3800,
Australia.

Mamoru Sugita
Center for Gene Research, Nagoya University, Nagoya 464-8602, Japan.

Mattias Thelander
Department of Plant Biology and Forest Genetics, Swedish University of
Agricultural Sciences, Uppsala SE-750 07, Sweden.

Kunihiko Ueda
Graduate School of Natural Science and Technology, Kanazawa University,
Kanazawa 920-1192, Japan.

Klaus von Schwartzenberg

Biozentrum Klein Flottbek und Botanischer Garten, Universität Hamburg,
Hamburg D-22609, Germany.

Takeshi Yoshimura
Graduate School of Natural Science and Technology, Kanazawa University,
Kanazawa 920-1192, Japan.

Andreas D. Zimmer
Plant Biotechnology, University of Freiburg, Freiburg D-79104, Germany.
PREFACE

When we received the invitation to write a book on Physcomitrella patens,

while it was yet another call on our time, the decision was in fact easily
made. All of us have been committed to showing the value of P. patens as a
model organism for most of our scientific careers and for the three of us this
covers over 70 years (one of us contributes 38 years to the total).
This is a timely publication. The selection of P. patens as the first non-
angiosperm land plant to have its genome sequenced and the reporting of
the sequence in Science in 2008 as part of an international collaboration are
amongst the best of recent significant advances in biological research.
We are fortunate to know the moss research community and the selection
of chapters and authors was relatively easy. Some of them come from a
long history of moss research, others attracted to the system have learned
of its utility by laboratories willingly sharing their expertise or by attending
practical workshops such as those held in Leeds in the late 1990s. It was in
1999 that the decision was made to meet annually and conferences have since
seen a steady increase in new interest and international collaborations.
The chapters included in this book cover a broad range, from those using
P. patens as a marker against other species for evolutionary or ecological
studies (Chapters 1, 2 and 3), to those investigating the unique features of P.
patens, for example gene targeting (Chapter 4), to those using moss, either as
a comparator for other organisms or because of the ease of study in moss, to
investigate standard biological processes (Chapters 5–12).
The chapters speak for themselves; however, in bringing them together,
there are some general comments to make. The first is one of nomenclature. As
described in the first sentence of Chapter 1, Physcomitrella patens is sometimes
known as Aphanorrhegma patens. The difference, according to Brent Mishler,
is a matter of opinion as to whether Physcomitrella is considered a different
genus to Aphanorrhegma, in which case Physcomitrella is the correct name,
but if the two are considered as the same genus, then Aphanorrhegma is the
correct name. Most taxonomists believe that they are different genera. Of
course, much of the research referred to in this book may eventually be able
to provide a definitive answer, but in the meantime, we will only refer to this
moss as Physcomitrella patens.
The second general point is one of terminology and particularly whether
mosses have leaves. The single-cell layer of cells with a primitive mid-rib is
commonly called a leaf but is clearly not equivalent to an angiosperm leaf.
Phyllode is sometimes used as an alternative for leaves but does not meet
the exact needs of the bryophytes. The proper word to describe the leaves

xiii
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