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NATO ASI Series Advanced Science Institutes Series
A series presenting the results of activities sponsored by the NA TO Science Committee, which aims at the dissemination of advanced scientific and technological knowledge, with a view to strengthening links between scientific communities.
The Series is published by an international board of publishers in conjunction with the NATO Scientific Affairs Division
A Life Sciences B Physics
C Mathematical and Physical Sciences
o Behavioural and Social Sciences
E Applied Sciences
F Computer and Systems Sciences
G Ecological Sciences H Cell Biology
Plenum Publishing Corporation London and New York
Kluwer Academic Publishers Dordrecht, Boston and London
Springer-Verlag Berlin Heidelberg New York London Paris Tokyo
Series H: Cell Biology Vol. 17
Cell to Cell Signals in Plant, Animal and Microbial Symbiosis
Edited by
Silvano Scannerini Dipartimento di Biologia Vegetale, Universita di Torino Viale Mattioli 25, 10125 Torino, Italy
David Smith University of Edinburgh, Old College South Bridge, Edinbourgh EH8 9YL, United Kingdom
Paola Bonfante-Fasolo Dipartimento di Biologia Vegetale, Universita di Torino Viale Mattioli 25, 10125 Torino, Italy
Vivienne Gianinazzi-Pearson INRA Station de Genetique et d'Amelioration des Plantes de Dijon B.v 1540, 21034 Dijon, France
Springer -Verlag Berlin Heidelberg New York London Paris Tokyo Published in cooperation with NATO Scientific Affairs Division
Proceedings of the NATO Advanced Research Workshop on Cell to Cell Signals in Plant, Animal and Microbial Symbiosis held at Villa Gualino, Torino, Italy, May 19-22, 1987
Library of Congress Cataloging-in-Publication Data. Cell to cell signals in plant, animal, and microbial symbiosis 1 edited by Silvano Scannerini ... [et al.l p. cm.-(NATO ASI series. Series H, Cell biology; vol. 17) "Proceedings ofthe NATO advanced research workshop held at Villa Gualino, Torino, Italy, May 19-22, 1987"-Tp. verso. "Published in cooperation with NATO Scientific Affairs Division." Includes index.
ISBN-13: 978-3-642-73156-3 e-ISBN-13: 978-3-642-73154-9 DO!: 10.1007/978-3-642-73154-9
1. Symbiosis-Congresses. 2. Cell interaction-Congresses. I. Scannerini, Silvano, 1940-.11. North Atlantic Treaty Organization. Scientific Affairs Division. III. Series. [DNLM: 1. Cell Communication. 2. Symbiosis-congresses. QH 548 C393 1987] QH548.C451988 574.5'2482-dc 19 DNLMIDLC for Library of Congress 88-6434
This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, re-use of illustrations, recitation, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. Duplication ofthis publication or parts thereof is only permitted under the provisions ofthe German Copyright Law of September 9, 1965, in its version of June 24, 1985, and a copyright fee must always be paid. Violations fall under the prosecution act of the German Copyright Law.
© Springer-Verlag Berlin Heidelberg 1988
Softcoverreprint of the hardcover 1st edition 1988
2131/3140-543210
This book is dedicated to the memory of Prof. Mario di Lullo,
secretary of the NATO Scientific Affairs Division.
PREFACE
In a mutualistic symbiosis, two (or sometimes more) organ
isms of very different kinds come together and establish a long
term association in which the partners show a high degree of
integration with each other. Studies have been made in various
types of symbiosis to understand the processes by which the
partners recognise each other, but hitherto there has been no
attempt to compare and correlate results from a broad range of
associations to see if any common principles emerge. Further
more, the previous lack of a comparative approach has led to
inconsistences in the way in which terms are used - even such
a fundamental term as 'recognition' itself.
There is frequently an assumption that molecular signals
pass between the partners in the early stages of the establish
ment of a symbiosis, although the experimental evidence under
lying this assumption requires critical evaluation. Because
contact between host and symbiont becomes intimate and often
morphologically complex, it may be difficult to get direct
biochemical evidence for the existence of signals, and heavy
reliance has to be placed on indirect evidence, especially as
provided by ultrastructural, cytochemical, immunological and
genetic studies.
For these various reasons, it was particularly opportune
to hold a NATO Advanced Workshop on cell-to-cell signals in
plant, animal and microbial symbiosis. The objective of the
workshop was to identify the processes involved in contact be
tween cells of hosts and symbionts. It involved critical re
views of the current state of knowledge of various symbiotic
systems, assessment of the evidence for signals, identification
of the topics worthy of further investigation, and evaluation
of the most promising experimental techniques which could be
used.
This book contains the papers which were presented at the
Workshop, which was held at the Villa Gualino, Torino, May
19-22, 1987.
Silvano Scannerini
David Smith
VIII
ACKNOWLEDGMENTS
In sending this book to print it is our pleasure and duty to thank the
institutions and people whose contribution has been essential for the achieve
ment of the workshop and of this volume.
First of all we must thank the NATO Scientific Affairs Division which
has granted us a generous contribution. In particular our thanks go, unfortu
nately posthumous, to prof. Mario di Lullo with whom the activity began, to
Dr. Alain Jubier who has substituted him and to the NATO Scientific Represe~
tative of our workshop: Prof. J.A. Fortin.
Thanks must also be expressed to the lSI (Institute for Scientific In
terchange) which has kindly hosted us at Villa Gualino; to Prof. Tullio
Regge president of lSI, Prof. M. Rasetti director, and also to the coopera
tion of Dr. Tiziana Bertoletti and the efficiency and patience of Ms. Carmen
Novella.
Thanks also to the University of Turin and to its Chancellor Prof. M.U.
Dianzani whose special grant has made possible the participation of people
from non-NATO countries. Among personnel and students of the Plant Biology
Department a special mention goes to Ms. Marina Beorchia for secretarial
work, Mr. Pantaleone Tripaldi for dealing with administration and Dr. Pietro
Spanu for translations.
S. Scannerini D.C. Smith P. Borfante V. Gianinazzi-Pearson
PARTICIPANTS
Albertano, P.
II Universita degli Studi di Roma "Tor Vergata", Dipartimento di
Biologia, Via O. Raimondo, 00173 (La Romanina) Roma, Italy.
Becard, G.
Universite Laval, Centre de Recherche en Biologie Forestiere,
Faculte de Foresterie et de Geodesie, G1K 7P4 Quebec, Canada.
Bermudes, D.
Boston University, Department of Biology, 2 Cummington Street,
Boston, Massachusetts, 02215 U.S.A.
Berta, G.
Universita di Torino, Dipartimento di Bio1ogia Vegetale, Viale
Mattioli 25, 10125 Torino, Italy.
Bertocchi, C.
Universita di Trieste,Dipartimento di BiochimiFa, Biofisica e
Chimica delle Macromolecole, P.le Europa 1, 34127 Trieste, Italy.
Bonfante, P.
Universita di Torino, Dipartimento di Biologia Vegetale, Viale
Mattioli 25, 10125 Torino, Italy.
Brewin, N.
John Innes Institute, AFRC Institute of Plant Science Research,
Department of Genetics, Colney Lane, Norwich NR4 7UH UK.
x
Callow, J.A.
The University of Birmingham, Department of Plant Biology, P.O. Box
363, Birmingham B15 2TT UK.
Cheli, F.
lTniversita degli Studi di Milano, Dipartimento di Biologia "Luigi
Gorini", Sezione di Botanica Sistematica, Via Celoria 26, 20133
Milano, Italy.
Codignola, A.
Universita degli Studi di Torino, Dipartimento di Biologia Vegetale,
Via1e Mattioli 25, 10125 Torino, Italy.
Dazzo, F.B.
Michigan State University, Department of Microbiology and Public
Health, Giltner Hall, East Lansing, Michigan 48824-1101 U.S.A.
De Vecchi, L.
Universita degli Studi di Milano, Dipartimento di Biologia "Luigi
Gorini", Sezione di Botanica Sistematica, Via Celoria 26, 20133
Milano, Italy.
Dorritie, B.
Boston University, Department of Biology, 2 Cummington Street,
Boston, Massachusetts, 02215 U.S.A.
Douglas, A.E.
John Innes Institute, AFRC Institute of Plant Science Research,
Department of Cell Biology, Colney Lane, Norwich NR4 7UH U.K.
XI
Fortin, J.A.
Universite Laval, Faculte de Foresterie et de Geodesie, Centre de
Recherche en Biologie Forestiere, Cite Universitaire, G1K 7P4
Quebec, Canada.
Galun, M.
Tel-Aviv University, Faculty of Life Sciences, Department of
Botany, Tel-Aviv, Israel.
Gianinazzi, S.
Institut National de la Recherche Agronomique, Station de Genetique
et d'Arnelioration des Plantes de Dijon, B.V. 1540, 21034 Dijon cedex,
France.
Gianinazzi-Pearson, V.
Institut National de la Recherche Agronomique, Station de Genetique
et d'Amelioration des Plantes de Dijon, B.V. 1540, 21034 Dijon cedex,
France.
Giovannetti, M.
Universita degli Studi di Pisa, Istituto di Microbiologia Agraria
e Tecnica, C.N.R., Centro di Studio per la Microbiologia del Suolo,
Via del Borghetto 80, 56100 Pisa, Italy.
Green, J.R.
The University of Birmingham, Department of Plant Biology, P.O. Box
363, Birmingham B15 2TT UK.
Grilli Caiola, M.
II Universita degli Studi di Roma "Tor Vergata", Dipartimento di
Biologia, Via 0. Raimondo, 00173 (La Romanina) Roma, Italy.
XII
Hinde, R.
The University of Sidney, School of Biological Sciences, Macleay
Building A12, NSW 2006.
Honegger, R.
Institut fur Pflanzenbiologie Cytologie, Zollikerstrasse 107,
CH-8008 Zurich.
Jones, J.L.
The University of Birmingham, Department of Plant Biology, P.O. Box
363, Birmingham, B15 2TT UK.
Lefebvre, F.
Institut National des Sciences Appliquees de Lyon, Laboratoire de
Biologie Appliquee, Batiment 406, 20 Avenue A. Einstein, 69621
Villeurbanne Cedex, France.
Maffei, M.
Department of Biological Chemistry, Washington State University,
Pullman, Washington, U.S.A.
Margulis, L.
Boston University, Department of Biology, 2 Cummington Street,
Boston, Massachusetts, 02215 U.S.A.
Martinotti, G.
Universita di Torino, Istituto di Microbiologia, Via Santena 9,
10126 Torino, Italy.
Massicotte, H.B.
University of Guelph, College of Biological Science, Department
of Botany, Guelph, Ontario, Canada N1G 2W1.
XIII
Matta, A.
Universita di Torino, Istituto di Patologia Vegetale, Via P. Giuria
15, 10125 Torino, Italy.
McAuley, P.J.
University of Oxford, Department of Plant Sciences, Agricultural
Science Building, Parks Road, Oxford OX1 3PF UK.
McFall-Ngai, M.J.
University of California San Diego, La Jolla, California, 92093 U.S.A.
Minganti, C.
Istituto Guido Donegani, Department of Biotechnology, Via G. Fauser
4, 28100 Novara, Italy.
Monsigny, M.
Laboratoire de Biochimie Cel1ulaire et Mo1eculaire des Glycoconjugues,
Centre de Biophysique Moleculaire du Centre National de la Recherche
Scientifique et U.F.R. de Sciences Fondamentales et App1iquees de
l'Universite d'Or1eans, 1 rue Haute, 45071 Orleans Cedex 2, France.
Nardon, P.
Institut National des Sciences Appliquees de Lyon, Laboratoire de
Biologie Appliquee, Batiment 406, 20 Avenue A. Einstein, 69621
Villeurbanne Cedex, France.
Nealson, K.H.
The University of Wisconsin-Milwaukee, Center for Great Lakes
Studies, 600 E. Greenfield Avenue, Milwaukee, Wisconsin U.S.A.
Noris, E.
Istituto Guido Donegani, Department of Biotechnology, Via G. Fauser
4, 28100 Novara, Italy.
XIV
Nuti, M.
Universita degli Studi di Padova, Dipartimento di Biotecnologie
Agrarie, Via Gradenigo 6, 35131 Padova, Italy.
Okker, R.J.H.
Department of Plant Molecular Biology, Botanical Laboratory,
Nonnensteeg 3 2311 VJ Leiden, The Netherlands.
Pasti, M.B.
Universita degli Studi di Padova, Dipartimento di Biotecnologie
Agrarie, Via Gradenico 6, 35131 Padova, Italy.
Perotto, S.
Centro di Studio sulla Micologia del Terreno del C.N.R., Viale
Mattioli 25, 10125 Torino, Italy.
Piche, Y.
Universite Laval, Faculte de Foresterie et de Geodesie, Cite
Universitaire, G1K 7P4 Quebec Canada.
Rahat, M.
The Hebrew University of Jeru3alem, The Institut of Life Sciences,
The Department of Zoology, 91904 Jerusalem, Israel.
Ray, T.C.
The University of Birmingham, Department of Plant Biology, P.O. Box
363, Birmingham, B15 2TT UK.
Reisser, W.
Fachbereich Biologie der Philipps-Universitat Marburg, Botanik,
D-3550 Marburg-Lahnberge.
CONTENTS
I. PHYSIOLOGY AND MORPHOLOGY OF CELL-TO-CELL INTERACTIONS
Cellular interactions between host and endosymbiont in
dinitrogen-fixing root nodules of woody plants ........................... l
J.G. Torrey
Recognition mechanisms in the Azolla-Anabaena symbiosis ........•........ 27
M. Grilli Caiola and P. Albertano
The functional morphology of cell-to-cell interactions in lichens ....... 39
R. Honegger
Host-fungus interactions in ectomycorrhizae ..................•.......... 55
Y. Piche, R.L. Peterson and H.B. Massicotte
Morphological integration and functional compatibility
between symbionts in vesicular arbuscular endomycorrhizal
associations .........................................................•.. 73
V. Gianinazzi-Pearson and S. Gianinazzi
Cell to cell interactions in insect endocytobiosis ....•..•.............. 85
P. Nardon
Luminescent bacteria: symbionts of nematodes and pathogens
of insects •..................................•........•................ 101
K. Nealson, T.M. Schmidt and B. Bleakley
Cell-to-cell interactions during the establishment of the
Hydra-Chlorella symbiosis .....................................•.•...•.. 115
P.J. McAuley
XVIII
Specificity in the Convoluta roscoffensis/Tetraselmis
symbiosis .....•...........•......................................•...... 131
A.E. Douglas
The cell structures of plant, animal and microbial symbionts,
their differences and similarities ...................................... 143
S. Scannerini
Symbiosis and evolution: a brief guide to recent literature ............. 159
L. Margulis and D. Bermudes
II. SIGNALS IN PLANTS
Molecular signals in plant cell recognition .....................•....... 167
J.A. Callow, T. Ray, T.M. Estrada-Garcia and J.R. Green
Early recognition signals in the Rhizobium trifolii-white
clover symbiosis .....................•...........................•...... 183
F.B. Dazzo, R.I. Hollingsworth, S. Philip-Hollingsworth,
K.B. Smith, M.A. Welsch, M. Djordjevic and B.G. Rolfe
Flavonoid compounds as molecular signals in Rhizobium-legume
symbiosis ..................................•.....•...•.................. 189
S.A.J. Zaat, H.P. Spaink, C.A. Wijffelman, A.A.N. van
Brussel, R.J.H. Okker and B.J.J. Lugtenberg
Soredia formation of compatible and incompatible lichen
symbionts ......•................................•....•.................. 207
M. Galun and J. Garty
XIX
The role of the cell wall as a signal in mycorrhizal
associations .........•.............................••................... 219
P. Bonfante-Fasolo
III. SIGNALS IN ANIMALS
Peptide and carbohydrate moieties as molecular signals
in animal cell recognition ...........................•...•.............. 237
M. Monsigny, A.C. Roche, C. Kieda, R. Mayer and P. Midoux
Genetical and biochemical interactions between the host and
its endocytobiotes in the weevils Sitophilus (Coleoptere,
Curculionidae) and other related species ................................ 255
P. Nardon and A.M. Grenier
Signals in the Paramecium Bursaria - Chlorella Sp. association .......... 271
W. Reisser
Nutritional interactions as signals in the green hydra symbiosis ........ 283
A.E. Douglas
The establishment of algal/hydra symbioses - A case of recognition
or preadaptation? ...................•.................................. 297
M. Rahat and V. Reich
Factors produced by symbiotic marine invertebrates which
affect translocation between the symbionts ....•..•...................... 311
R. Hinde
xx
Specificity in dinomastigote-marine invertebrate
symbioses: an evaluation of hypotheses of mechanisms
involved in producing specificity ...•..........•........................ 325
R.K. Trench
IV. RECOMMENDATIONS FOR FUTURE RESEARCH AND APPLICATIONS
Applications of genetic engineering to "Symbiontology" in
agricul ture ............................................................. 347
M.P. Nuti, M.B. Pasti and A. Squartini
The application of monoclonal antibody technology to the
study of cell-cell interactions ......................................... 361
J.R. Green, J.L. Jones and J.A. Callow
The use of monoclonal antibodies to investigate plant
microbe interactions in pea root nodules containing
Rhizobium leguminosarum •................................................ 373
N.J. Brewin, D.J. Bradley, E.A. Wood, E.L. Kannenberg,
K.A. VandenBosch, G.W. Butcher
Immunocytochemical studies of symbiotic development and
metabolism in nitrogen-fixing root nodules ..........••.................. 385
K.A. VandenBosch
Concepts leading to an understanding of recognition and
signalling between hosts and symbionts ..................•............... 397
D.C. Smith
SUBJECT INDEX ..............................•.•.......................... 409