1 Interrelationships of the Cereal Cyst Nematode
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pi,- t.. 1 INTERRELATIONSHIPS OF THE CEREAL CYST NEMATODE, HETERODERA AVENAE, AND THE TAKE-ALL FUNGUS, OPHIOBOLUS GRAMINIS ON BARLEY. Roger Cook Department of Zoology and Applied Entomology, Imperial College of Science and Technology. A thesis submitted for the degree of Doctor of Philosophy of the University of London. 2 ABSTRACT Observations on a number of field populations of the cereal cyst nematode, Heterodera avenae and the take-all fungus, Ophiobolus graminis, on barley, suggested a relationship between the two, in which higher nematode populations were associated with low incidence of take-all. The level of root invasion by H. avenae and multiplication of the nematode showed this relationship with the fungus. Further observations, in which the number of eggs per cyst was negatively correlated with level of take-all infection suggested one explanation of the relationship. The effects of 0. graminis on H. avenae were studied in a series of pot experiments. In the presence of high levels of take-all the multiplication of natural populations of the nematode was depressed, and this was associated with reductions in the number of eggs per cyst. Experiments in sterilised soil showed that production of cysts and their contents were decreased by take-all. Smaller cysts were produced on plants infected with O. graminis. On take-all infected plants the rate of development of the nematode was slower and the ratio of males to females produced was higher than on uninfected plants. Take-all appeared to affect the sex determination of larvae, fewer females developing in infected roots. Invasion of barley roots by H. avenae larvae was reduced by prior infection with O. Araminis. In none of the experiments was the degree or severity of take-all affected by the presence of the nematode. 4 ACKNOWLEDGEMENTS I wish to thank Professors O.W. Richards and T.R.E. Southwood for permission to work in their department. I owe much to the encouragement and advice of Dr. N.G.M. Hague who supervised the work presented in this thesis. Officers of the National Agricultural Advisory Service, Reading, gave valuable assistance, particularly during the early stages of my field work, To these, and the farmers whose fields I visited,I express my gratitude. Especial thanks go to my wife who typed this thesis and gave me every support. The project was financed by an Agricultural Research Council grant, which I gratefully acknowledge. 5 TABLE OF CONTENTS Page Title Page 1 Abstract 2. Acknowledgements 4 Table of Contents 5 SECTION I Introduction 7 SECTION II A Field Observations, 1967 16 B Field Observations, 1969 37 SECTION III A Pot experiments with field soils 1. Introduction 45 2. Materials and methods 46 3. Experimental details and results a Effect of adding 0. graminis to H. avenae populations in eight field soils 51 b Effect of adding O. graminis to three populations of H. avenae in one field soil ▪ • 59 c Effect of O. graminis on Meloidogve naasi in naturally infested soil 66 d Resistance of oats to O. graminis in the presence of three nematode populations 73 4. Discussion 79 B Pot experiments in sterilised soil 1. Introduction 82 2. Materials and methods 82 3. Experimental details and results a Effects of three levels of O. graminis on final populations of H. avenae 84 b Effect of O. graminis on invasion of roots and development of H. avenae 88 4. Discussion 96 Page SECTION IV Further studies on the effects of 0. graminis on development of H. avenae 1. Introduction 100 2. Experimental details and results a Experiment 1 100 b Experiment 2 106. 3. Discussion 111 SECTION V Further studies on the effects of O. graminis on the invasion of barley roots by H. avenae. 1. Introduction 116 2. Experimental details and results a Effect of level of take-all infection on invasion of roots by. H. avenae 117 b Invasion of barley roots by H. avenae in relation to the position of a take-all lesion • • 120 c Invasion by H. avenae of healthy roots of take-all infected root systems 124 d Attraction of H. avenae larvae to take-all infected barley roots 125 3. Discussion 128 SECTION VI General discussion and conclusions 131 References 149 Appendix tables 162 SECTION I Introduction This thesis presents the results of investigations into the interrelationships between Ophiobolus Framinis Saco., the causal fungus of the take-all disease, and Heterodera avenge Woll., the cereal cyst nematode, on their common host, barley. Both the nematode and fungus are soil borne pathogens of cereals and have become of greater economic importance as a result of changes in British agriculture since the Second World War. Increased cereal production has resulted in cereals being grown in shorter rotations and in some regions they are grown continuously on the same land. Large acreages of barley are grown continuously in farming areas relatively close to Imperial College Field Station, so that it was convenient to study the relationship between take-all and the cereal cyst nematode on barley. The fungus 0. graminjs causes the take-all disease of cereals. In the field the disease appears as more or less circular patches of stunted unthrifty plants. Under dry summer conditions severely infected plants may die prematurely and the ears of these plants have a bleached appearance. However roots may be infected with take-all with- out the plant shavang obvious above ground symptoms. The grain produced on infected plants is small and shrivelled so that yields may be much reduced. At maturity the root systems are blackened and rotted and considerable secondary invasion by weakly parasitic or saprophytic fungi occurs. Infection takes place when roots come into contact with mycelium of the fungus, which has overwintered in the soil on plant debris infected the previous season. Coarse dark hyphae produce a network around the root surface and fine hyaline hyphae penetrate the roots. Garrett (1934) has called these hyphae, runner and infection hyphae, respectively. The infection procedure has been described by Fellows (1928) on wheat and proceeds in a similar fashion on barley. Runner hyphae develop on the epidermis and, from these, infection hyphae arise and grow radially through the cortex and into the stele. Spread of the fungus occurs only by contact with the root, when it spreads longitudinally along the outside and in the stele of the root (Garrett, 1942). Rotting of the cortical tissues produces dark lesions which may girdle the roots. Take-all is considered the most important root rot of cereals and considerable yield losses are attributable to it (Garrett,19423 Lester,1967). Conditions of intensive wheat or barley cultivation favour the build up of high levels of take-all, through reducing the period which the fungus must survive saprophytically in the soil, between its parasitic phases on cereal hosts. Some loss of the overwintering inoculum of take-all occurs during this phase of saprophytic survival, but inevitably in cereal monoculture, higher initial levels of inocula remain to infect successive crops (Garret & Mann,1948). It was feared that the increasing practice of cereal monoculture would lead to serious losses due to take-all, and that the disease might be a serious threat to the future of cont- inuous cereal growing. These fears have been justified to a large extent (Lester,1967). However, considerable evidence has been accumulated to suggest that cereals may be grown continuously in Umny cases without maintaining economically unacceptable levels of take-all. This phenomenon has been described as "take-all decline" (Slope & Cox,1964). Shipton (1967) has established the "decline" phenomenon on a range of fields and also provided experimental proof. It appears that after four or five continuous cereal crops take-all reaches peak levels, and declines under succeeding crops to a level which is acceptable to farmers. It has proved profitable to continue growing cereals through the years of maximum take-all, to take advantage of the higher yields of subsequent crops. Evidence from several sources indicates that under conditions of continuous cereal production, a soil microflora antagonistic to 0. graminis develops 10 and this may be responsible for u1 aecline of the disease (Ehle,1966; Skipsna,1960; Zogg,1960). H. avenae, the cereal cyst nematode, is also parasitic on cereals. The life cycle of the nematode has been described by Franklin (1951). Larvae invade the host roots during spring and become sedentary within the root. In response to infection, the roots produce "giant cells", by division of cells and dissolution of cell walls. These are limited to the stefe and provide the nematode with a feeding site at which it remains throughout its development. The larvae grow and moult three times before reaching maturity. Males emerge from the root to fertilise the females. These remain attached to their feeding site, but exposed to the soil through the rupturing of the cortex, caused by their growth. After fertilisation the female produces eggs, which eventually pack all the space inside the female body wall. This hardens and thickens and it is in this encysted state that the nematodes survive the winter. After a period of inactivity the eggs hatch and the larvae invade the host roots in the spring. Although winter oats have been found infected by the larvae in autumn, there is only one gener- ation of H. avenae produced each year on spring sown cereals (Gair,1965). Symptoms of cereal cyst nematode attack are a slight swelling of the infected root, accompanied by branching. 11 Severely infected plants have shallow, much branched root systems whose efficiency is much impaired. In heavily infested soil, plants may be stunted and die, or produce only poorly filled grain.