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Biology and Histopathology of Different 1 BIOLOGY AND HISTOPATHOLOGY OF DIFFERENT ISOLATES OF ANGUINA TRITICI ON TRITICUM SPP. by Riadh Falih Al-Sabie B.Sc. (Baghdad), DIC. (Imperial College), M.Sc. (London) A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN THE FACULTY OF SCIENCE, UNIVERSITY OF LONDON. Department of Zoology and Applied Entomology Imperial College at Silwood Park Imperial College of Science and Technology AshursE Lodge Sunninghill Ascot Berkshire: ENGLAND September, 1980. 11 ABSTRACT Isolates of Anguina tritici from Australia, England, India, Iraq and U.S.A. were maintained on spring wheat. Measurements of males and females and second stage juveniles (J2) showed consistent morphometric differences between some isolates. Host range studies on species and varieties of Triticwn and AegiZops indicated an ability to infect a wide range of hosts of which 9 were new records. Infection studies on naturally infected wheat revealed that the growing point was invaded by the second stage juveniles shortly after flower induction. Artificial inoculation of wheat plants showed that the infective stage needed an association with the flower primordia for at least 24 days (latent period) for galling to be initiated. Further studies were made on the effect of temperature on invasion and distribution of galls in artificially inoculated heads. The histopathology of infection and subsequent gall development was observed. J2 invaded the primordia of either one stamen only (outer anther), ovary only or both to form the gall. The J2 survived in the soil for 250 days in the absence of a host, and some could still infect and form galls after 225 days. J2 from all isolates could not survive for more than 40 days in aerated water. Further studies were made on survival of J2 in the field in either presence or absence of the host. By monitoring the change in length of J2 in different molar concen- tration of NaCl, it was found that all isolates had a very limited ability to osmoregulate (0.05-0.1 M NaC1). Respiration rate of J2 varied with temperature and different isolates had different temperature optima for respiration. The oxygen consumption of all isolates was totally inhibited by 10-4 M NaC N,followed by death within 15 minutes. ACKNOWLEDGEMENTS I wish to express my gratitude to Dr. A.A.F. Evans for his valuable guidance, supervision and advice throughout this research, and for his interest and help during the preparation of the manuscript. Without his invaluable encouragement this work would not have been possible. I should also like to acknowledge with thanks the helpful suggestions given by Dr. W.M. Hominick, D.J. Wright and J. Bridge, and also to F. Awan for reading part of the manuscript. My thanks to Miss. O.M. Goss, Department of Agriculture, Western Australia; Dr. G. Swarup, Indian Agricultural Research Institute; Dr. J.N. Sasser, North Carolina State University, U.S.A.; and the staff of the Department of Plant Pathology, Abu-Ghraib, Iraq, for supplying the wheat galls of Anguina tritici isolates; and also to Dr. V. Chapman, Plant Breeding Institute, Cambridge, and the staff of Kew Gardens, London, for supplying the wheat varieties collection. Thanks are due to Mr. R.G. Davies and Dr. S. Young for their help in statistical analysis, and Mr. P. Nicholas for his help with photo- graphy, and the rest of the staff of the Imperial College, Silwood Park for the various ways in which they assisted. I am immensely grateful to my wife, Basima, for her tolerance, patience, understanding and moral encouragement throughout the duration of this work, and my special thanks to my parents and all the family. Finally, I take the opportunity to thank the Iraqi Government for the scholarship from the Ministry of Higher Education and Scientific Research, which has enabled me to pursue this work. iv TABLE OF CONTENTS Page Title page i Abstract Acknowledgements Table of contents iv SECTION I INTRODUCTION AND LITERATURE REVIEW 1. a. Introduction 1. b. Historical view 2. c. Classification 4. d. Identification 5. e. Morphometrics 7. f. Distribution and host range ___ 10. g. Biology and life history --- 11. h. Development of Anguina tritici --- 13. i. Biochemistry and survival of Anguina tritici --- 15. j. Effect of Anguina tritici on biochemistry in wheat --- --- 17. k. Associated with other pathogens --- 18. 1. Control --- 20. m. Aims and objective of the present study 22. SECTION II GENERAL MATERIALS AND METHODS 23. SECTION III STUDIES ON MORPHOLOGY AND HOST RANGE WITHIN ANGUIIVA TRITICI --- 25. A. A Comparison of 'Morphological Variation Within and Between Isolates of A. tritici 25. 1. Introduction --- 25. 2. Materials and methods __- 26. 3. Results --- 29. v Page B. Host Range and Host Suitability Within Isolates of A. tritici 51. 1. Introduction 51. 2. Materials and Methods 51. 3. Results 54. C. Discussion 66. SECTION IV HISTOPATHOLOGY AND THE INFECTION PROCESS 73. 1. Introduction 73. 2. Materials and Methods 74. 3. Results 75. 4. Discussion 93. SECTION V FACTORS AFFECTING THE INFECTION PROCESS OF A. TRITICI IN WHEAT 96. 1. Introduction 96. 2. Inoculation before the double ridge stage 96. a. Materials and Methods 96. b. Results 96. 3. Inoculation during and after flower induction 97. a. Materials and Methods 97. b. Results 97. 4. Inoculation throughout the year using successive generations 97. a. Materials and Methods 97. b. Results 98. 5. The density of artificial inoculum 98. a. Materials and Methods 98. b. Results 101. vi Page 6. Transfer of inoculum from one plant to another during the period of inoculation 105. a. Materials and Methods 105. b. Results 105. 7. Wheat c.v. MMaris Dove inoculated with Anguina spp. from Holcus mollis (creeping soft grass) and creeping soft grass with A. tritici 106. a. Materials and Methods 106. b. Results 106. 8. Galls produced on naturally infested host under field conditions 108, a. Materials and Methods 108. b. Results 108. 9. Discussion 108. SECTION VI SURVIVAL OF SECOND STAGE JUVENILES UNDER DIFFERENT CONDITIONS 115. 1. Introduction 115. 2. Survival of J2 under field conditions in the absence of the host. a. Materials and Methods b. Results 3. Survival of J2 under field conditions in the presence of the host a. Materials and Methods b. Results 4. Survival of J2 in different media with temperatures and their subsequent infectivity 123. a. Materials and Methods 123, b. Results 124. vii Page 5. Survival of J2 in air saturated water 129. a. Materials and Methods 129. b. Results 129. 6. Discussion 131. SECTION VII OXYGEN CONSUMPTION OF ANGUINA TRITICI OF SECOND STAGE JUVENILES OF DIFFERENT ISOLATES 135. 1. Introduction 135. 2. Oxygen consumption of J2 from single and mixed galls of the U.K. and Iraqi isolates 135. a. Materials and Methods 135. b. Results 138. 3. Oxygen consumption at different temperatures of J2 from mixed galls of each isolate 141. a. Materials and Methods 141. b. Results 141. 4. The effect of different concentrations of aqueous NaCN on the oxygen consumption of J2 of A. tritici --- 143. a. Materials and Methods 143. b. Results 144. 5. Discussion 144. SECTION 'VIII EFFECT OF OSMOTIC STRESS ON SECOND STAGE JUVENILES OF DIFFERENT ISOLATES 147. 1. Introduction 147. 2. Materials and Methods 147. 3. .Results 148. 4. Discussion 156. SECTION IX GENERAL DISCUSSION ---- --- 159. References 166. Appendices 179. SECTION I INTRODUCTION AND LITERATURE REVIEW a. Introduction Nematodes are probably the most numerous multicellular animals in the world (Stockli, 1946), and are found in nearly every bio- logical niche that will support life (Cobb, 1914). The majority are non-parasitic and free-living in fresh or salt water or in soil, where they feed on micro-organisms such as bacteria, fungi and algae. However, nematodes have been found to be parasites on virtually all animal and plant life. They can cause great physical discomfort and debilitation .to man and his domestic animals as well as a variety of plant diseases that take their toll of crop production. In the past, nematode damage to crops was often ignored or att- ributed to other causes, such as lack of soil fertility, deficient soil moisture or "soil exhaustion". Nevertheless, they escaped notice because most kinds are too small to be seen without the aid of a microscope. Nematodes feed on the roots, crown, stems, leaves and even on the growing point (buds and root tips), of many crop plants. Among the plant parasitic nematodes, there are many genera where the response of the plant to invasion is the formation of galls on various parts of the plant. Amongst these gall-forming nematodes, the genus Anguina (Scopoli, 1777) causes galls on the above-ground parts of the plant. Frequently the form and location of the galls are charac- teristic of the nematode species. Anguina spp. are obligate plant parasites causing galls on floral structures or leaves of host plants. 2. The association of the genus Anguina with gall formation on grasses has been known for just over a century and a half (Needham, 1744), when it was described as galls in the flowers on a Gramin- aceous host. There is only one older record of plant damage by nematodes on wheat due to Anguina tritici (Steinbuch, 1799; Chitwood, 1935). Galls . were formed in place of seeds, and infection decreased grain yield, sometimes by as much as 60% (Anon., 1964). As wheat is the most important food crop grown by western man, occupying about 515 million acres, it is easy to appreciate the potential importance of such an organism. The nematode Anguina tritici is well known throughout most of the world as the wheat nematode, wheat gall nematode or ear-cockle nematode (Caveness, 1964). It is the longest known plant nematode and has been spread through infested seed to all wheat - growing regions of the world.
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