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POTATO VIRUS Y by NIKOLAOS KATIS

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POTATO VIRUS Y by NIKOLAOS KATIS STUDIES ON APHID TRANSMISSION OF POTATO VIRUS Y by NIKOLAOS KATIS (B .S c.) Thesis submitted to the University of London for the degree of Doctor of Philosophy Plant Pathology Department Rothamsted Experimental Station Harpenden, Herts* AL5 2JQ November 1984 2 ABSTRACT Two strains of potato virus Y (PVY) are common in potato crops. The ordinary stra in (PVY^) induces leaf drop streak in many potato cultivars followed by severe mosaic and vein clearing in tobacco, and the tobacco veinal necrosis strain (PVY N) induces mild mosaic in almost all potato cultivars and veinal necrosis in tobacco. PVYN did not affect the concentration of PVY° but PVY^ supress- ed PVY N in doubly infected plants of tobacco cv. White Burley and potato cv. King Edward, especially in plants kept at 30°C. At this temperature, no PVY N was recovered from doubly infected plants, which developed a slight mosaic although veinal necrosis appeared in two days on transfer to a cool glasshouse. The cereal aphid Rhopalosiphum padi (L.) transmitted both strains of PVY from and to both tobacco and potato, although much less frequently than did Myzus persicae (Sulz.) even when aphids making single probes were compared. R, padi and M. persicae retained PVY for similar duration. Both apterae and alatae of R. padi transmitted infrequently as also did progenies of individual R. padi that had transmitted PVY. M. persicae frequently inoculated both PVY 0and PVY N after a single probe into a doubly infected plant. Inefficient vectors (M. euphorbiae (Thomas) and R. padi) inoculated both strains much less frequently than M. persicae suggesting that they inoculated less virus. Access of M. persicae to oil treated, doubly infected leaves resulted in some preferential reduction in transmission of both PVY 0 and PVY N m. comparison with the untreated ones only 24-36 h after application, 3 M. persicae which probed a PVY N- or a beet mosaic virus (BMV)- infected leaf either before or after access to a PVY0-infected leaf were less likely to transmit PVY° than aphids which probed uninfected leaves. Transmission of BMV was similarly inhibited by aphids prob- ing a PVY N -infected leaf. However, transmission of PVY N was unaffect­ ed by whether or not M, persicae also probed a PVY°- or a BMV-infected leaf. Transmission of PVY 0 and PVY N was also unaffected by whether or not M. persicae also probed leaves infected with the non-aphid transmissible virus tobacco mosaic. Retention of PVY ,0 PVY Nand BMV by M. persicae was similar as was the effect of temperature on retent- ion of PVY 0 and PVY N by the same aphid species. In laboratory tests with glasshouse-grown potato plants cv. King Edward, M. persicae acquired PVY as readily from plants inoculat* ed 20 days previously as from secondarily-infected ones. With PVY° this was also the case when plants were inoculated young. Twenty days after inoculation. M. persicae acquired PVY 0 and PVY Nfrom plants of five potato cultivars differing in resistance to PVY and also from eight other isolates of PVY 0 and PVY N. Field potato plants of cvs. Record and King Edward inoculated with either PVY 0 or PVY Nearly in the growing season acted as foci for further spread although initially they were poorer sources than plants grown from infected tubers. No PVY was detected in any wild plant growing in or near a plot of PVY-infected potatoes. In 1984, alate aphids were trapped downwind of a plot of PVY- infected potato plants at Rothamsted. A total of 3969 alates were trapped, 2.57. of which infected test plants with PVY. Brachycaudus 4 helichrysi (Kltb.), flying early in the growing season, accounted for ca. 787. of transmissions and was probably the most important vector of PVY at Rothamsted that year. From early to mid-July M. persicae, and from mid-July to 8 August Phorodon humuli (Schrank) and Aphis spp., transmitted PVY most frequently. In this experiment, Metopolophium festucae (Theobald), Myzaphis rosarum (Kltb.), My 2us myosotodis (Borner) and Sitobion fragariae (Wlk.) were identified as vectors of PVY for the first time. 5 Contents Page ABSTRACT 2 Contents 5 List of Tables 9 L ist of Figures 12 List of Plates 13 List of virus abbreviations 15 ACKNOWLEDGEMENTS 17 1. GENERAL INTRODUCTION 19 2. REVIEW OF THE LITERATURE 24 2.1 Nonpersistent transmission of plant viruses by aphids 24 a. Introduction 24 b. Characteristics of nonpersistent transmission 25 c. Virus groups transmitted nonpersistently 28 d. Physical properties of nonpersistent viruses 29 e. The role of helper component 29 f. Sites of virus acquisition and inoculation in plant 32 g. Sites of transmitted virus in/on the aphid 33 h. Vector specificity 36 2.2 Transmission of potyviruses by non-colonizing aphids 37 3. GENERAL MATERIALS AND METHODS 46 3.1 Virus isolates 46 3.2 Plants 46 3.3 Aphids 46 3.4 Techniques 51 a. Virus acquisition and transmission by aphids 51 6 Page b. Manual transmission of viruses 51 c. Immunosorbent electro n microscopy (ISEM) 51 d. Enzyme-linked immunosorbent assay (ELISA) 52 e. Electron microscopy 53 3.5 Statistical analysis 53 EXPERIMENTAL WORK 54 4. INTERACTION OF PVY° AND PVYN IN DOUBLY INFECTED PLANTS 54 4.1 Interaction of PVY 0 and PVYN in glasshouse-grown tobacco plants* 54 4.2 Interaction of PVY0 and PVYN in glasshouse-potato p lan ts. 55 4.3 Interaction of PVY0 and PVYN in tobacco plants grown at different temperatures. 55 5. TRANSMISSION OF PVY° AND PVYN FROM DOUBLY INFECTED PLANTS 63 5.1 Acquisition of PVY 0 and PVYN by M. persicae after a single probe on a doubly infected tobacco leaf. 63 5.2 Acquisition of PVY 0 and PVY N by M. persicae> M. euphorbiae and R. padi from doubly infected potato p lan ts. 66 5.3 Transmission of PVYN by M. persicae and M. euphorbiae that initially fail to transmit. 73 5.4 Effect of oil on acquisition of PVY 0 and PVY Nfrom doubly infected tobacco. 76 6. EXPERIMENTS TESTING FOR INTERFERENCE BETWEEN VIRUSES OR VIRUS STRAINS DURING APHID TRANSMISSION 85 6.1 Experiments testing for interference between PVY0 and PVYN during sequential transmission by M. persicae. 85 6.2 Experiments testing for interference between BMV, PVY 0 and PVY^ during sequential transmission by M. persicae. 89 6.3 Experiments testing the ability of BMV from N. clevelandii and sugarbeet to inhibit transmission of PVY^ during sequential transmission by M. persicae. 94 7 Page 6*4 Experiments testing for interference between PVY , PV\fN and TMV during sequential transmission by M. persicae. 100 6.5 Cross-protection tests 101 6.6 Comparison of electrophoretic mobility of PVY0 , PVY N and BMV by gel-electrophoresis. 104 VIRUS RETENTION BY M. PERSICAE 114 7.1 The retention period of PVY^, PVY^ and BMV by M. persicae. 114 7.2 Effect of temperature on the retention of PVY° and PVYn by M. persicae. 118 ROLE OF WEEDS AS PVY SOURCES 121 PRIMARILY-INFECTED PLANTS AS SOURCES OF PVY 127 9.1 Acquisition of PVY O and PVY N by M. persicae from primarily infected potato cv. King Edward inoculated at different ages. 131 9.2 Acquisition of PVY O and PVYN by M. persicae from primarily infected potato plants of different c u ltiv a rs. 132 9.3 Acquisition of different isolates of PVY O and PVY N by M. persicae from primarily infected potato cv. King Edward plants. 135 9.4 Acquisition of PVY 0 and PVYN by M. persicae from different leaves of primarily infected potato plants cv. King Edward 137 9. 5 Field experiment 139 TRANSMISSION OF POTATO VIRUS Y BY CEREAL APHIDS 146 10.1 Transmission of PVY by R. padi, M. dirhodumt S. avenae and M. persicae. 147 10.2 Duration of acquisition access. 148 10.3 Transmission of PVY by apterae and alatae R. padi. 148 10.4 Transmission of PVY^ and PVY^. 150 10.5 Transmission of PVY to and from potato and tobacco. 150 8 Page 10.6 Retention of infectivity by R. padi and M. persicae. 151 10.7 Transmission of PVY by R. padi and M. persicae after a single probe. 151 10.8 Transmission of PVY by progeny of known vector R. padi. 154 11. SPREAD OF PVY BY APHIDS 158 12. GENERAL DISCUSSION 177 13. APPENDIX 185 14. REFERENCES 189 9 List of Tables Table Page 1. Transmission of potyviruses by non-colonizing aphids. 39 2. Test plants used in experiments for virus identif­ ication and assay. 47 3. Transmission of PVY 0 and PVY N by M. persicae or sap from singly and doubly infected tobacco cv. White Burley plants. 57 4. Transmission of PVY 0 and PVY N from singly and doubly infected potato cv. King Edward plants by manual inoculation of sap diluted to 10"^. 58 5. Sap transmission of PVY0 and PVYN from singly and doubly infected tobacco cv. White Burley plants kept at different temperatures. 61 6. Numbers of plants infected with PVY 0 and/or PVY Nby M. persicae allowed a single probe into doubly infected tobacco cv. White Burley. 65 7. Transmission of PVY 0 and PVY N from doubly infected potato cv. King Edward by different aphid species. 70 8. The analysis of variance of numbers of plants infected w ith PVY0 , PVYN or PVY0 + PVYN by M. persicae, M. euphorbiae and R. padi. 71 9. Transmission of PVYN by aphids that either transmitted (A) or failed to transmit (B) in the previous test. 75 10. Transmission of PVY 0 and PVYN from oil-treated and untreated doubly infected tobacco by M.
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