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Cyst Nematodes

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This book is a compendium of current information on all aspects of these economically important parasites. It provides comprehensive coverage of their biology, management, morphology and diagnostics, in addition to up-to-date information on molecular aspects of taxonomy, host-parasitic relationships and resistance. Written by a team of international experts,ÊCyst NematodesÊwill be invaluable to all researchers, lecturers and students in nematology, parasitology, agriculture and agronomy, industries with an interest in chemical and biological control products for management of plant-parasitic nematodes, and any courses, quarantine and advisory services.

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1 Cyst Nematodes – Life Cycle and Economic Importance



Cyst Nematodes – Life Cycle and Economic Importance

Maurice Moens1,2, Roland N. Perry2,3 and John T. Jones2,4,5

Flanders Research Institute for Agriculture, Fisheries and Food, Merelbeke,

Belgium; 2Ghent University, Ghent, Belgium; 3University of Hertfordshire, Hatfield,

Hertfordshire, UK; 4The James Hutton Institute, Invergowrie, Dundee, UK;


University of St Andrews, St Andrews, UK


1.1 Introduction

1.2 Impact

1.3  History of the Genus

1.4 Distribution

1.5 Identification

1.6  Life Cycle

1.7 Syncytium

1.8  Effect of Abiotic Factors

1.9  Important Species

1.10  Pathotypes and Races

1.11 Symptoms

1.12 Management

1.13 References

1.1 Introduction

Cyst nematodes are remarkable parasites. They have highly specialized interactions with plants and induce the formation of a unique feeding structure, the syncytium, within the roots of their hosts. Cyst nematodes are of enormous economic importance throughout the world and the various species infect all of the world’s most important crops (Jones et al., 2013); they also share a unique feature: the ability of the female to turn her cuticle into a durable, protective capsule for her eggs. Cyst nematodes are classified within eight genera of the subfamily Heteroderinae: Heterodera, Globodera, Cactodera, Dolichodera, Paradolichodera, Betulodera, Punctodera and


2 Genomics and Transcriptomics – a Revolution in the Study of Cyst Nematode Biology



Genomics and Transcriptomics – a

Revolution in the Study of Cyst Nematode


Sebastian Eves-van den Akker1,2 and John T. Jones3,4,5

Division of Plant Sciences, College of Life Sciences, University of Dundee,

Dundee, UK; 2Department of Biological Chemistry, John Innes Centre, Norwich

Research Park, Norwich, UK; 3The James Hutton Institute, Invergowrie, Dundee,

UK; 4The University of St Andrews, North Haugh, St Andrews, UK; 5Ghent

­University, Ghent, Belgium


2.1 Introduction

2.2  A Note of Caution

2.3 �Current Status of Genome and Transcriptome Projects for

Cyst Nematodes and Other Plant-parasitic Nematodes�

2.4  Key Findings from Genome/Transcriptome Projects

2.5  Population Genetics and Metagenetics

2.6  Identification of Key Biochemical Pathways and Targets for Control

2.7  Mitochondrial Genomes

2.8  Horizontal Gene Transfer

2.9 Accessibility

2.10  Conclusions and Future Prospects


3 Hatch, Survival and Sensory Perception




Hatch, Survival and Sensory


Edward P. Masler1 and Roland N. Perry2,3

USDA-ARS, Beltsville, Maryland, USA; 2University of Hertfordshire,

Hatfield, UK; 3Ghent University, Ghent, Belgium

3.1 Introduction

3.2  Biology of Hatching

3.3 Survival

3.4  Sensory Perception

3.5  Conclusions and Future Prospects

3.6 References

3.1 Introduction

The need to understand the functional biology of nematodes is central both to fundamental science and to practical aspects. Research on the biology of economically important cyst nematodes frequently has the declared aim of identifying novel control targets based on disruption of the nematode life cycle. The knowledge from such research also provides a fascinating exposition of the complex aspects of host–parasite interactions and the sophisticated mechanisms involved. In this chapter we focus on three aspects, hatching, survival and sensory perception, and explore the links among them and the associated interfaces between the cyst nematodes and their hosts.


4 Biology of Effectors



Biology of Effectors

John T. Jones1,2,3 and Melissa G. Mitchum4

The James Hutton Institute, Invergowrie, Dundee, UK; 2The University of

St Andrews, North Haugh, St Andrews, UK; 3Ghent University, Ghent, Belgium;


University of Missouri, Columbia, Missouri, USA


4.1 Introduction

4.2  Degradation of the Plant Cell Wall

4.3  Suppression of Host Defences

4.4  Manipulation of Host Biochemistry for Feeding Site Induction

4.5  Conclusions and Future Prospects

4.6 Acknowledgements

4.7 References

4.1 Introduction

4.1.1  What are effectors?

A wide range of definitions of effectors has been proposed by various authors, with varying degrees of inclusivity. For the purposes of this article we will use a deliberately broad definition as suggested by Hogenhout et al. (2009): ‘all pathogen (i.e. nematode) proteins and small molecules that alter host-cell structure and function’.

­Effectors in cyst nematodes need to fulfil a variety of functional roles, and each of these is considered in detail below. Effectors allow nematodes to overcome the physical barrier presented by the plant cell wall so that they can invade their hosts and migrate to a place suitable for induction of the feeding site. Effectors are required to suppress host defence responses and to protect the nematode from toxic compounds produced as a part of these responses. Many of these functional requirements are shared with effectors


5 Biochemistry


5 Biochemistry

David J. Chitwood and Edward P. Masler

USDA-ARS, Beltsville, Maryland, USA

5.1 Introduction

5.2 Lipids

5.3 Carbohydrates

5.4 Proteins

5.5  Conclusions and Future Prospects

5.6 References

5.1 Introduction

Part of the framework for effective control or management of cyst nematodes is the detailed understanding of their biology. There is also the fascination in examining mechanisms and their interactions from a purely academic perspective to acquire new knowledge. Some of the information on individual components of the biological system is dated. There is a paucity of research directly examining aspects of biochemistry, perhaps because of the difficulties associated with the microscopic size of cyst nematodes as experimental animals, and perhaps because funding agencies have not viewed these areas of research as top priority.

However, burgeoning genomic data now provide opportunities to make inferences about biochemical pathways through bioinformatic analyses of nematode gene content and expression. There are numerous genome projects, either completed or in progress, and the emphasis is on how the genes and the proteins


6 Role of Population Dynamics and Damage Thresholds in Cyst Nematode Management



Role of Population Dynamics and

Damage Thresholds in Cyst Nematode


George W. Bird1, Inga A. Zasada2 and Gregory L. Tylka3

Michigan State University, East Lancing, Michigan, USA; 2USDA-ARS, Corvallis,

Oregon, USA; 3Iowa State University, Ames, Iowa, USA


6.1 Introduction

6.2  Heterodera schachtii (Sugar Beet Cyst Nematode)

6.3  Globodera spp. (Potato Cyst Nematodes)

6.4  Heterodera glycines (Soybean Cyst Nematode)

6.5  The Rest of the Heteroderinae

6.6  Conclusions and Future Prospects

6.7 References

6.1 Introduction

Nematode population dynamics and damage thresholds are applied aspects of population ecology. The domain of population ecology had its origins in the works of Lotka (1925) and

Volterra (1926), leading to the contributions of  Lack (1954) and Huffaker (1958). With the publication of Odum’s Fundamentals of Ecology

(1959), the basic principles and concepts pertaining to organization at the species population level were established. Currently, population ecology is a vibrant discipline, essential for developing a true understanding of how ecosystems work (Rockwood, 2015). It involves how a definable group of individuals of a single species interact with the biotic and abiotic attributes of their environment.


7 Quarantine, Distribution Patterns and Sampling




Quarantine, Distribution Patterns and Sampling

Jon Pickup1, Adrian M.I. Roberts2 and Loes J.M.F. den Nijs3

Science and Advice for Scottish Agriculture, Edinburgh UK; 2Biomathematics and

Statistics Scotland, Edinburgh, UK; 3National Plant Protection Organisation/

Netherlands Food and Consumer Product Safety Authority, Wageningen,

The Netherlands

7.1 Introduction

7.2 Quarantine

7.3  Phytosanitary Status

7.4  Soil Sampling

7.5  Laboratory Diagnosis

7.6  Conclusions and Future Prospects

7.7 References

7.1 Introduction

Under the guidelines set out within the International Standard on Phytosanitary Measures

(ISPM) 16 (FAO, 2002), quarantine pest status implies that specific regulations are implemented to ensure that phytosanitary measures address all transmission pathways to ensure that such pests are not introduced into or spread within the country, and that, if found, official control measures are implemented with the aim of eradication or containment. It is generally the responsibility of individual countries to make decisions of whether a pest is treated as a quarantine species.


8 Mechanisms of Resistance to Cyst Nematodes



Mechanisms of Resistance to Cyst Nematodes

Aska Goverse and Geert Smant

Laboratory of Nematology, Wageningen University, The Netherlands

8.1 Introduction

8.2  Basal Immunity to Cyst Nematodes

8.3  Host-specific Immunity to Cyst Nematodes

8.4  Quantitative Aspects of Host-specific Immunity

8.5  Transcriptional Reprogramming and Defence Gene Expression

8.6  Hormone-mediated Defence Responses by Cyst Nematodes

8.7  Conclusions and Future Prospects

8.8 References









8.1 Introduction

conserved microbial-derived components or danger signals by so-called pattern recognition

Plants are constantly under attack by a wide receptors (PRR). However, pathogens have range of pathogens and pests including bacteria, evolved strategies to overcome basal immunity. viruses, fungi, oomycetes, insects and nematodes. To counteract these virulent pathogens, plants


9 Resistance Breeding



Resistance Breeding

Vivian C. Blok1, Gregory L. Tylka2, Richard W. Smiley3, Walter S. de Jong4 and Matthias Daub5


The James Hutton Institute, Dundee, UK; 2Iowa State University, Ames, Iowa,

USA; 3Oregon State University, Pendleton, Oregon, USA; 4Cornell University,

Ithaca, New York, USA; 5Julius Kühn-Institut, Braunschweig, Germany

9.1 Introduction

9.2  Resistance and Tolerance

9.3  Sources of Resistance and Genetics

9.4  Virulence, Pathotypes and Races

9.5  Screening (Phenotyping)

9.6  Cereal Cyst Nematodes

9.7  Potato Cyst Nematodes

9.8  Soybean Cyst Nematodes

9.9  Sugar Beet Cyst Nematodes

9.10  Other Cyst Nematodes

9.11  Conclusions and Future Prospects

9.12 References

9.1 Introduction

Cyst nematodes cause serious economic losses to the world’s four most important food crops:

­cereals (wheat, maize and rice) and potatoes, as well as to important cash crops such as soybean and sugar beet. Due to a lack of obvious or distinct symptoms on the aerial parts of the host plants resulting from nematode parasitism of the roots, combined with the requirements for specific isolation processes and specialist skills to identify plant-parasitic nematodes, there is often a lack of awareness of their presence and the losses they can cause. This can be particularly problematic in subsistence agriculture where multiple contributing factors and a lack of nematological expertise can compromise attributing crop damage to plant-parasitic nematodes.


10 Plant Biotechnology Approaches: From Breeding to Genome Editing



Plant Biotechnology Approaches:

From Breeding to Genome Editing

Godelieve Gheysen1 and Catherine J. Lilley2

Department of Biotechnology, Ghent University, Belgium; 2Centre for Plant Sciences,

University of Leeds, UK


10.1 Introduction

10.2  PCR and Next Generation Sequencing

10.3 �Molecular Research into Plant–Nematode Interactions:

Using Molecular Biology to Understand the Parasite�

10.4  Genetic Engineering: The Basic Principles

10.5  Breeding or Genetic Engineering with Natural Resistance Genes

10.6 �Genetic Engineering Using Genes that Interfere with

Nematode Feeding and Digestion�

10.7 �Secretion of Peptide Repellents from Root Tips Inhibits

Nematode Invasion�

10.8  RNAi Acting across Kingdom Borders�

10.9 �Susceptibility Genes as an Alternative Target for

Nematode Resistance�

10.10 �Genome Editing Can Adapt Susceptibility Genes with Surgical Precision�


11 Biological Control of Cyst Nematodes through Microbial Pathogens, Endophytes and Antagonists


11  Biological Control of Cyst Nematodes through Microbial Pathogens, Endophytes and Antagonists

Keith G. Davies1,2, Sharad Mohan3 and Johannes Hallmann4

University of Hertfordshire, Hatfield, UK; 2Norwegian Institute of Bioeconomy

Research, Ås, Norway; 3Indian Agricultural Research Institute, New Delhi, India;


Julius Kühn-Institut Federal Research Centre for Cultivated Plants, Münster,



11.1 Introduction

11.2  Nematophagous and Antagonistic Fungi

11.3  Rhizobacteria and Root Endophytic Bacteria

11.4  Microbial–Nematode Molecular Interactions

11.5  Biological Control Products

11.6  Managing Biological Control

11.7  Conclusions and Future Prospects

11.8 References

11.1 Introduction

The biological control of nematode pests has a long history dating back at least to the 1930s when Linford and his colleagues showed that the natural enemies of plant-parasitic nematodes restricted their population growth (Linford, 1937;


12 Interactions with Other Pathogens



Interactions with Other Pathogens

Horacio D. Lopez-Nicora and Terry L. Niblack

Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA

12.1 Introduction

12.2  Defining Interactions

12.3 �Methodologies for Investigation of Interactions between

Nematodes and Other Organisms

12.4  Biological and Statistical Evidence of Interactions

12.5  Mechanisms of Interactions

12.6  Interactions between Cyst Nematodes and Other Organisms

12.7  Conclusions and Future Prospects

12.8 References

12.1 Introduction

Interactions between nematodes and other organisms are one component of the vast ecological network of biotic and abiotic interactions with plants. Quantifying the effect of each component alone is not easy and multiple components (‘determinants’) present larger challenges

(Wallace, 1978, 1989). Complex interactions between plant-parasitic nematodes and other pathogenic organisms generate uncertainties in our abilities to predict host damage. The lack of comprehension of the mechanisms of these interactions and under- or overestimation of damage and economic thresholds impede the development and implementation of management strategies.


13 Field Management and Control Strategies



Field Management and Control


Matthew A. Back1, Laura Cortada2, Ivan G. Grove1 and Victoria Taylor3

Harper Adams University, Newport, UK; 2International Institute of Tropical

­Agriculture, Nairobi, Kenya; 3Arcis Biotechnology, Daresbury Innovation Centre,

Sci-Tech Daresbury, Darebury, UK


13.1 Introduction

13.2  Cultural Control Methods for Cyst Nematodes

13.3 Biofumigation

13.4  Trap Cropping and Natural Resistance

13.5  Use of Plant Biomass, Oils and Extracts

13.6  Application of Biological Control Agents

13.7  Agrochemical Control of Cyst Nematodes

13.8  Conclusions and Future Prospects

13.9 References

13.1 Introduction

Globally, cyst nematode species are recognized for causing serious damage in a broad diversity of crops including, but not exclusively, soybean, potatoes, cereals, carrots, beet, peas, rice, brassicas, grapes and tobacco. In a review by Jones et  al. (2013), cyst nematodes (Globodera and


14 General Morphology of Cyst Nematodes



General Morphology of Cyst


James G. Baldwin1 and Zafar A. Handoo2

University of California, Riverside, California, USA; 2USDA, ARS, BARC-West,

Beltsville, Maryland, USA


14.1 Introduction

14.2  Egg and Embryo

14.3  Second- to Fourth-stage Juveniles

14.4 Males

14.5 Females

14.6 Cysts

14.7 Techniques

14.8  Minimal Standards for Species Descriptions

14.9  Conclusions and Future Prospects

14.10 References

14.1 Introduction

Within Tylenchomorpha, including most plant-­ parasitic nematodes, cyst nematodes (Heteroderinae) are morphologically distinctive among

Hoplolaimidae1 consistent with adaptations for sedentary parasitism and the capacity for dormancy or suspended development. Most important among these adaptations is the cyst, a structure that evolved within heteroderids2 and that has been defined as ‘a persistent tanned sac which retains eggs and is derived from some or all components of the mature female body wall’ (Luc et al., 1986). Although this type of cyst is unique to heteroderids, convergent morphological adaptations for sedentary parasitism


15 Taxonomy, Identification and Principal Species



Taxonomy, Identification and

Principal Species

Zafar A. Handoo1 and Sergei A. Subbotin2, 3

USDA, ARS, Beltsville, Maryland, USA; 2California Department of Food and

Agriculture, Sacramento, California, USA; 3Center of Parasitology of A.N.

Severtsov Institute of Ecology and Evolution, Moscow, Russia


15.1 Introduction

15.2 Identification

15.3  Systematic Position

15.4  Subfamily Heteroderinae Diagnosis

15.5 Genus Heterodera Schmidt, 1871

15.6  Subfamily Punctoderinae Diagnosis

15.7 Genus Globodera Skarbilovich, 1959

15.8 Genus Punctodera Mulvey & Stone, 1976

15.9 Genus Cactodera Krall & Krall, 1978

15.10 Genus Dolichodera Mulvey & Ebsary, 1980

15.11 Genus Betulodera Sturhan, 2002

15.12 Genus Paradolichodera Sturhan, Wouts & Subbotin, 2007

15.13 Genus Vittatidera Bernard, Handoo, Powers, Donald & Heinz, 2010

15.14  Conclusions and Future Prospects

15.15 Acknowledgements


16 Molecular Taxonomy and Phylogeny



Molecular Taxonomy and Phylogeny

Sergei A. Subbotin1,2 and Andrea M. Skantar3

Plant Pest Diagnostic Center, California Department of Food and Agriculture,

California, USA; 2Center of Parasitology of A.N. Severtsov Institute of Ecology and

Evolution, Moscow, Russia; 3USDA, ARS, Beltsville, Maryland, USA


16.1 Introduction


16.2  Nuclear Ribosomal RNA Genes


16.3  Nuclear Protein-coding Genes


16.4  Mitochondrial DNA Genome Organization


16.5  Origin and Phylogeny of Heteroderidae


16.6  Phylogeny and Phylogeography of Punctoderinae


16.7  Phylogeny and Phylogeography of Globodera 410

16.8  Co-evolution of Cyst Nematodes with their Host Plants


16.9  Conclusions and Future Prospects


16.10 References


16.1 Introduction

For many years evolutionary relationships among species and genera of cyst nematodes were estimated by classical comparison of morphological characters. Since the 1990s molecular information, such as nucleotide, amino acid sequences and restriction fragment length


17 Biochemical and Molecular Identification



Biochemical and Molecular


Lieven Waeyenberge

ILVO, Flanders Research Institute for Agriculture, Fisheries and Food, Merelbeke, Belgium

17.1  Statutory and Non-statutory Issues

17.2  Biochemical and Molecular Identification

17.3  Conclusions and Future Prospects

17.4 References

17.1  Statutory and Non-statutory


The International Plant Protection Convention

(IPPC) was founded on 6 December 1951 at the

6th Conference of the Food and Agriculture

­Organization of the United Nations (FAO-UN). Its mission is ‘to secure cooperation among nations in protecting global plant resources from the spread and introduction of pests of plants, in order to preserve food security, biodiversity and to facilitate trade’ ( To consolidate the objectives of the IPPC, National Plant Protection

Organizations (NPPOs) were initiated or further fortified. These organizations developed their own plant health regulations in agreement with the principles of the World Trade Organizations



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