Cell to Cell Signals in Plant, Animal and Microbial Symbiosis

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