MOLECULAR AND PHYSIOLOGICAL BASISOF NEMATODE SURVIVAL

MOLECULAR AND PHYSIOLOGICAL BASIS OF NEMATODE SURVIVAL To Clare and Ann, whose support and patience have been essential for our careers in nematology. MOLECULAR AND P HYSIOLOGICAL BASIS OF NEMATODE SURVIVAL Edited by Roland N. Perry Plant Pathology and Microbiology Department, Rothamsted Research, Harpenden, Hertfordshire, UK and Biology Department, Ghent University, Ghent, Belgium and David A. Wharton Department of Zoology, University of Otago, Dunedin, New Zealand CABI is a trading name of CAB International CABI Head Offi ce CABI North American Offi ce Nosworthy Way 875 Massachusetts Avenue Wallingford 7th Floor Oxfordshire OX10 8DE Cambridge, MA 02139 UK USA Tel: +44 (0)1491 832111 Tel: +1 617 395 4056 Fax: +44 (0)1491 833508 Fax: +1 617 354 6875 E-mail: cabi@cabi.org E-mail: cabi-nao@cabi.org Website: www.cabi.org ©CAB International 2011. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Molecular and physiological basis of nematode survival/edited by Roland N. Perry and David A. Wharton. p. cm. Includes bibliographical references and index. ISBN 978-1-84593-687-7 (alk. paper) 1. Nematodes Physiology. 2. Nematodes Adaptation. I. Perry, R. N. (Roland N.) II. Wharton, David A. QL391.N4M55 2011 571.1’257 dc22 2010033015 ISBN-13: 978 1 84593 687 7 Commissioning editor: Nigel Farrar Production editor: Fiona Chippendale Typeset by SPi, Pondicherry, India. Printed and bound in the UK by CPI Antony Rowe, Chippenham. v Contents About the Editors xiii Contributors xv Preface xvii 1 Survival of Parasitic Nematodes outside the Host 1 Roland N. Perry and Maurice Moens 1.1 Introduction 1 1.2 Survival of Life Cycle Stages 2 1.2.1 The egg 2 1.2.2 Egg packaging 4 1.2.3 Larval stages 5 1.2.4 Adults 6 1.2.5 Dauer forms 7 1.3 Hatching and Dormancy 9 1.4 Behavioural Adaptations 11 1.5 Water Dynamics 13 1.5.1 Dehydration 13 1.5.2 Rehydration 18 1.6 Implications for Control Options 19 1.7 Conclusions and Future Directions 21 1.8 References 22 2 Survival of Plant-parasitic Nematodes inside the Host 28 Jose Lozano and Geert Smant 2.1 Introduction 28 2.2 Morphological Adaptations to Plant Parasitism 29 vi Contents 2.2.1 Cuticle, surface coat and cuticular camouflage 29 2.2.2 The oral stylet – a multi-tool for nematodes 31 2.2.3 Pharyngeal glands – the source of all evil 31 2.3 Molecular and Physiological Adaptations to Plant Parasitism 32 2.3.1 Host invasion 32 2.3.2 Feeding behaviour and structures 35 2.3.3 Plant innate immunity 36 2.3.4 PAMP-triggered immunity 36 2.3.5 Effector-triggered immunity 37 2.4 Molecular and Cellular Phenomena in Plant Innate Immunity to Nematodes 40 2.4.1 Defence genes: phytoalexins, pathogenesis-related proteins and protease inhibitors 40 2.4.2 Pathogenesis-related proteins 42 2.4.3 Protease inhibitors 43 2.4.4 Cell wall fortifications with callose deposits and lignin 43 2.4.5 Hypersensitive response and programmed cell death 44 2.5 Immune Modulation by Nematodes in Plants 48 2.5.1 Detoxification of reactive oxygen species (ROS) and modulation of ROS signalling 48 2.5.2 Modulation of plant hormone balance and secondary metabolism 49 2.5.3 Modulation of lipid-based defences 50 2.5.4 Modulation of calcium signalling 51 2.5.5 Modulation of host protein turnover rate 52 2.5.6 Modulation of host immune receptors 53 2.5.7 Cross-kingdom modulation 54 2.6 Conclusions and Future Directions 55 2.7 Acknowledgements 55 2.8 References 56 3 Survival of Animal-parasitic Nematodes inside the Animal Host 66 Richard Grencis and William Harnett 3.1 Introduction 66 3.2 Gastrointestinal-dwelling Nematodes 66 3.2.1 Gastrointestinal nematode infection – chronicity is the norm 67 3.2.2 The immune response to gastrointestinal nematodes – can it be protective? 68 3.2.3 Immunoregulation during chronic infection – a necessary compromise? 70 3.2.4 Trichinella, a gut- and tissue-dwelling nematode that bucks the trend 72 Contents vii 3.3 Filarial Nematodes 73 3.3.1 Adaptation to changes in environment 73 3.3.2 Immunomodulation during filarial nematode infection 75 3.3.3 Defined filarial nematode molecules known to modulate the immune system 77 3.3.3.1 Cystatins 77 3.3.3.2 Dirofilaria immitis-derived antigen 77 3.3.3.3 ES-62 77 3.4 Conclusions and Future Directions 78 3.5 References 79 4 The Genome of Pristionchus pacificus and Implications for Survival Attributes 86 Matthias Herrmann and Ralf J. Sommer 4.1 Introduction 86 4.2 Pristionchus–Beetle Interactions and Biogeography 88 4.2.1 Diplogastridae–insect interactions 88 4.2.2 Pristionchus–beetle interactions 88 4.2.3 Pristionchus pacificus is a cosmopolitan species 90 4.3 Behaviour and Chemoattraction 90 4.4 Pristionchus–Bacterial Interactions 91 4.5 From Genetics to Genomics 91 4.5.1 Expansion of detoxification machinery 92 4.5.2 Cellulases and horizontal gene transfer 93 4.5.3 The evolution of parasitism and the role of ‘pre-adaptations’ 94 4.6 The Analysis of Pristionchus pacificus Dauer Regulation Provides Inroads for the Study of Parasitism 95 4.7 Conclusions and Future Directions 96 4.8 Acknowledgements 97 4.9 References 97 5 The Dauer Phenomenon 99 Warwick Grant and Mark Viney 5.1 Introduction 99 5.2 Initiating Dauer Development 101 5.2.1 Environmental signals 101 5.2.2 The chemistry of dauer induction 103 5.2.3 Sensory biology and ecology of dauer signals 105 5.2.4 Dauer signalling and the ecology of the dauer phenomenon 106 5.3 Genetic Variation in Dauer Switching 109 5.4 The Biology of the Dauer Stage 111 5.5 Dauer as a Pre-adaptation for the Evolution of Parasitism in Nematodes 113 5.5.1 Dauer biology and parasitism 113 5.5.2 Dauer molecular biology and parasite evolution 116 5.6 Conclusions and Future Directions 119 5.7 Acknowledgements 120 5.8 References 120 6 Gene Induction and Desiccation Stress in Nematodes 126 Ann M. Burnell and Alan Tunnacliffe 6.1 Introduction 126 6.2 The Effects of Water Loss on Living Systems 127 6.3 Protein Homeostasis 130 6.4 Membrane Integrity in Anhydrobiotic Nematodes 135 6.5 Oxidative Stress and its Effects during Desiccation and Anhdyrobiosis 138 6.6 Stabilizing Nucleic Acids 140 6.7 Model Nematodes for Anhydrobiosis Studies 141 6.8 Conclusions and Future Directions 143 6.9 Acknowledgements 146 6.10 References 146 7 Longevity and Stress Tolerance of Entomopathogenic Nematodes 157 Parwinder S. Grewal, Xiaodong Bai and Ganpati B. Jagdale 7.1 Introduction 157 7.2 Longevity of Infective Juveniles 159 7.3 Factors Affecting Longevity of Infective Juveniles 160 7.3.1 Stored energy reserves 160 7.3.2 Temperature 161 7.3.3 Desiccation 162 7.3.4 Hypoxia 164 7.4 Physiological Mechanisms of Longevity and Stress Tolerance 164 7.4.1 Physiology of longevity 164 7.4.2 Physiology of temperature tolerance 164 7.4.3 Physiology of desiccation tolerance 167 7.4.4 Physiology of hypoxia tolerance 169 7.5 Genetic Selection for Temperature and Desiccation Tolerance 169 7.6 Molecular Mechanisms of Desiccation Tolerance 170 7.7 Identification of Longevity and Stress Tolerance Genes 172 7.7.1 Longevity genes 172 7.7.2 Stress tolerance genes 172 7.8 Conclusions and Future Directions 175 7.9 References 176 viii Contents 8 Cold Tolerance 182 David A. Wharton 8.1 Introduction 182 8.2 Cold Tolerance Strategies 183 8.2.1 How many strategies? 183 8.2.2 What is the dominant strategy of nematode cold tolerance? 186 8.2.3 Ice nucleation 188 8.3 Cold Tolerance Mechanisms 189 8.3.1 Phenotypic plasticity 189 8.3.2 Changes in phospholipid saturation 191 8.3.3 Heat shock proteins 191 8.3.4 Organic osmolytes 192 8.3.5 Ice-active proteins 193 8.3.6 Other mechanisms of cold tolerance 194 8.4 Linking Mechanisms to Strategies 195 8.4.1 The role of trehalose 196 8.4.2 Stress proteins in cold tolerance 197 8.5 Conclusions and Future Directions 198 8.6 References 198 9 Molecular Analyses of Desiccation Survival in Antarctic Nematodes 205 Bishwo N. Adhikari and Byron J. Adams 9.1 Introduction 205 9.2 Molecular Anhydrobiology of Antarctic Nematodes 206 9.3 Stress Response System 208 9.3.1 Constitutively expressed genes 209 9.3.2 Stress-induced genes 212 9.3.2.1 Late embryogenesis abundant proteins 212 9.3.2.2 Small heat shock proteins 213 9.3.2.3 Ubiquitin 215 9.4 Signal Transduction System 216 9.5 Metabolic System 217 9.6 Oxidative Stress Response and Detoxification System 219 9.7 Cryoprotectant 221 9.8 Cross-tolerance and Stress-hardening 223 9.9 Conclusions and Future Directions 225 9.10 Acknowledgements 226 9.11 References 227 10 Thermobiotic Survival 233 Eileen Devaney 10.1 Introduction 233 10.2 Temperature Regulates Development in Nematodes 234 10.3 How Does Caenorhabditis elegans Sense Temperature? 235 Contents ix 10.4 Temperature Sensing in Parasitic Nematodes 237 10.5 Heat Shock Factor – the Master Regulator of the Heat Shock Response 238 10.6 Integration of the Stress Response and Developmental Pathways 240 10.7 Heat Shock Protein Families 242 10.7.1 Hsp90 243 10.7.2 The small heat shock protein family 245 10.7.3 Hsp70 246 10.8 Conclusions and Future Directions 247 10.9 Acknowledgements 249 10.10 References 249 11 Osmotic and Ionic Regulation 256 David A. Wharton and Roland N. Perry 11.1 Introduction 256 11.2 Osmotic and Ionic Regulation in Nematodes 257 11.2.1 Measuring internal osmotic concentration, water flux and volume changes 257 11.2.2 The importance of balanced salt solutions 260 11.2.3 Osmoconformers or osmoregulators? 261 11.2.4 Hyperosmotic or hyposmotic regulation? 261 11.2.5 Ionic regulation 263 11.3 Avoidance of Osmotic Stress 266 11.4 Survival of Extreme Osmotic/Ionic Stress 267 11.5 Mechanisms of Osmotic Regulation 268 11.5.1 Excretory structures and osmoregulation 268 11.5.2 Cuticular permeability 269 11.5.3 The operation and control of osmoregulatory mechanisms 270 11.5.4 Aquaporins 273 11.6 Conclusions and Future Directions 274 11.7 Acknowledgements 275 11.8 References 275 12 Biochemistry of Survival 282 John Barrett 12.1 Introduction 282 12.2 Proteins and Enzymes 283 12.2.1 Temperature and protein stability 283 12.2.2 Enzymes in hot- and cold-adapted animals 284 12.2.3 Proteins and hydrostatic pressure 285 12.2.4 Stress proteins 286 12.2.4.1 Heat shock proteins (molecular chaperones) 286 x Contents [...]... desiccation survival and the link to nematode dispersion This link and the need to understand the temporal factors involved in survival are clearly vital for effective management and control options for parasitic nematodes The pre-adult stages of nematodes are called juveniles by plant nematologists, and the term infective juvenile (IJ) is favoured by researchers working with entomopathogenic nematodes... desirable for research on nematodes to become more integrated in the future Roland N Perry and David A Wharton April 2010 1 Survival of Parasitic Nematodes outside the Host ROLAND N PERRY1 AND MAURICE MOENS2 1Rothamsted Research, Harpenden, Hertfordshire, UK and Biology Department, Ghent University, Ghent, Belgium; 2Institute for Agricultural and Fisheries Research, Merelbeke, Belgium and Laboratory for Agrozoology,... the remarkable structural, physiological and behavioural adaptations that facilitate desiccation survival (Perry, 1999) However, more recently the molecular aspects have received considerable attention, and these are reviewed by Burnell and Tunnacliffe, Chapter 6, and Adhikari and Adams, Chapter 9, this volume In this chapter, we examine the morphological, physiological and behavioural adaptations,... primarily on nematode survival physiology, hatching, sensory perception and behaviour Several of his past PhD and postdoctoral students are currently involved in nematology research He co-edited The Physiology and Biochemistry of Free-living and Plantparasitic Nematodes (1997), the textbook Plant Nematology (2006), and Root-knot Nematodes (2009) He is author or co-author of over 40 book chapters and refereed... organizers invited us to arrange and coordinate a session entitled Survival, adaptation and tolerance of nematodes in extreme environments’ This gave us the opportunity of inviting speakers from different areas of nematology, and the discussion during the session, and subsequently, convinced us that there was a need for a book on nematode survival that combined information on nematodes from all groups The... some species of nematode to survive desiccation for periods considerably in excess of the duration of the normal life cycle has ©CAB International 2011 Molecular and Physiological Basis of Nematode Survival (eds R.N Perry and D.A Wharton) 1 2 R.N Perry and M Moens been studied in detail, in part because in species with a direct life cycle this attribute is linked to effective dispersion of nematodes In... long-term anhydrobiosis depends on subsequent biochemical and molecular adaptations (see Burnell and Tunnacliffe, Chapter 6, and Adhikari and Adams, Chapter 9, this volume) The majority of free-living stages of animal- and plant-parasitic nematodes belong to the external dehydration strategists and show little intrinsic ability to control water loss and survive desiccation, being dependent on high relative... the L4 and large numbers of this stage aggregate The L4 have several behavioural, morphological and physiological attributes that combine to provide an astonishing ability to survive extreme desiccation (Perry 1977a,b,c; see Section 1.5) The rice stem nematode, Ditylenchus angustus, is adapted to more humid habitats and there is no specific survival stage L3, L4 and adults have only limited survival. .. several heat shock proteins and an enhanced resistance to desiccation (Kenyon, 1997) The factors initiating dauer formation act on the L1 and early L2 and include food availability, temperature and levels of a C elegans-specific pheromone (Riddle and Albert, 1997) Grant and Viney (Chapter 5, this volume) discuss the dauer phenomenon in the context of nematode life history strategies and evolution, with particular... survive, using a variety of behavioural, physiological and morphological adaptations Anguina spp inhabit the aerial parts of cereals and forage grasses and invade ovules, where they induce galls, mate and lay eggs, and the L2 accumulate in the galls, where they can survive dry for many years By contrast, the survival stage of Ditylenchus dipsaci is the L4, and in adverse conditions, especially at the