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Symptom Recovery in Tomato Ringspot Virus Infected Nicotiana

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Symptom Recovery in Tomato Ringspot Virus Infected Nicotiana SYMPTOM RECOVERY IN TOMATO RINGSPOT VIRUS INFECTED NICOTIANA BENTHAMIANA PLANTS: INVESTIGATION INTO THE ROLE OF PLANT RNA SILENCING MECHANISMS by BASUDEV GHOSHAL B.Sc., Surendranath College, University of Calcutta, Kolkata, India, 2003 M. Sc., University of Calcutta, Kolkata, India, 2005 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) August 2014 © Basudev Ghoshal, 2014 Abstract Symptom recovery in virus-infected plants is characterized by the emergence of asymptomatic leaves after a systemic symptomatic phase of infection and has been linked with the clearance of the viral RNA due to the induction of RNA silencing. However, the recovery of Tomato ringspot virus (ToRSV)-infected Nicotiana benthamiana plants is not associated with viral RNA clearance in spite of active RNA silencing triggered against viral sequences. ToRSV isolate Rasp1-infected plants recover from infection at 27°C but not at 21°C, indicating a temperature-dependent recovery. In contrast, plants infected with ToRSV isolate GYV recover from infection at both temperatures. In this thesis, I studied the molecular mechanisms leading to symptom recovery in ToRSV-infected plants. I provide evidence that recovery of Rasp1-infected N. benthamiana plants at 27°C is associated with a reduction of the steady-state levels of RNA2-encoded coat protein (CP) but not of RNA2. In vivo labelling experiments revealed efficient synthesis of CP early in infection, but reduced RNA2 translation later in infection. Silencing of Argonaute1-like (NbAgo1) genes prevented both symptom recovery and RNA2 translation repression at 27°C. Also, translation repression was compromised in Rasp1-infected wild-type (WT) plants grown at 21°C. NbAgo1 and NbAgo2 mRNAs accumulated to similar levels at 21°C and 27°C in mock-inoculated WT plants. Both genes were induced during Rasp1 infection. Interestingly, the effect of silencing NbAgo2 on Rasp1 infection was only evident at low temperatures resulting in higher accumulation of CP. Taken together, our results suggest that although both NbAgo1 and NbAgo2 genes are induced, recovery of Rasp1-infected plants at ii 27°C is associated with an NbAgo1-dependent mechanism that represses the translation of viral RNA2. In contrast, recovery of GYV-infected plants is associated with a reduction of viral RNA and CP levels at both temperatures. Moreover, silencing of either NbAgo1 or NbAgo2 did not prevent recovery of GYV-infected plants at 21°C. However, both GYV-infected NbAgo1 and NbAgo2-silenced plants accumulated higher level of CP in recovered leaves compared to control plants. In conclusion, this study identifies translation repression as a novel regulatory mechanism in recovery and suggests that different mechanisms may operate during recovery in an isolate and/or temperature-dependent manner. iii Preface The research work described here is a result of the work done in Dr. Hélène Sanfaçon’s lab from May 2009 to March 2014 by the candidate. Below is a list of manuscripts (published or in preparation) that comprise this thesis. The contribution of the candidate is mentioned below. Chapter 1: Literature review The candidate wrote the chapter and Dr. Hélène Sanfaçon provided editorial support. Chapter 2: Temperature-dependent symptom recovery in Nicotiana benthamiana plants infected with tomato ringspot virus is associated with reduced translation of viral RNA2 and requires ARGONAUTE 1 was modified from the manuscript: Ghoshal, B. and Sanfaçon, H. (2014) Temperature-dependent symptom recovery in Nicotiana benthamiana plants infected with tomato ringspot virus is associated with reduced translation of viral RNA2 and requires ARGONAUTE 1. Virology 456-457: 188-197 The candidate designed, performed the research and wrote the manuscript. Dr. Hélène Sanfaçon supervised the work and manuscript preparation and provided editorial support. iv Chapter 3: Possible involvement of both NbAgo1 and NbAgo2 genes during ToRSV infection in a temperature-dependent manner , a version of this chapter will be prepared for publication. The candidate designed, performed and wrote the chapter. Dr. Hélène Sanfaçon supervised the work and provided editorial support. Chapter 4: Symptom recovery of ToRSV-GYV infected plants at 21°C is concomitant with low accumulation of viral products and is not prevented in NbAgo1- silenced plants, a version of this chapter will be prepared for publication. The candidate designed, performed and wrote the chapter. Dr. Hélène Sanfaçon supervised the work and provided editorial support. The sequencing of the entire genome was done by Joan Chisholm, Melanie Walker, Ting Wei, Basudev Ghoshal, and Hélène Sanfaçon. Chapter 5: General discussion The candidate wrote the chapter and Dr. Hélène Sanfaçon provided editorial support. v Table of Contents Abstract ....................................................................................................................................... ii Preface ....................................................................................................................................... iv Table of Contents ....................................................................................................................... vi List of Tables ............................................................................................................................. ix List of Figures ............................................................................................................................. x List of Abbreviations ................................................................................................................ xii Acknowledgments .................................................................................................................... xv Dedication .............................................................................................................................. xviii Chapter 1: Literature review ................................................................................................... 1 1.1 Introduction ....................................................................................................... 1 1.2 Multiplication cycle of positive-sense single-strand RNA virus ...................... 3 1.3 RNA silencing in plants .................................................................................... 7 1.3.1 Description of the pathway ...................................................................... 7 1.3.2 Characteristics of the key components in the pathway .......................... 10 1.3.2.1 Dicer/Dicer like enzymes .......................................................... 12 1.3.2.2 Argonaute .................................................................................. 12 1.3.2.3 RNA dependent RNA Polymerase ............................................ 13 1.3.2.4 Types of small RNA .................................................................. 15 1.4 RNA Silencing as an antiviral defence response in plants and its counter defence .............................................................................................. 17 1.4.1 Role of RNA silencing components in antiviral defence response ....... 18 1.4.2 Mode of RISC activity - Cleavage or translation repression of the viral RNA............................................................................................... 22 1.4.3 Counteracting RNA silencing – Viral suppressors ................................ 26 1.5 Symptom development, maintenance and recovery during plant-virus interaction ...................................................................................................... 29 1.5.1 Symptom development, maintenance and RNA silencing .................... 31 1.5.2 Symptom recovery ................................................................................. 34 1.5.2.1 Role of RNA silencing in symptom recovery ........................... 35 1.5.2.2 Role of suppressors in meristem entry of viruses and symptom recovery .................................................................... 36 1.5.2.3 Effect of temperature on symptom recovery ............................. 38 1.5.2.4 Recovery and the nature of host and virus isolate ..................... 39 1.6 Overview of Tomato ringspot virus ................................................................ 40 1.6.1 Classification of ToRSV ........................................................................ 41 1.6.2 Genome organization and proteins encoded by ToRSV ....................... 41 vi 1.6.3 ToRSV multiplication cycle .................................................................. 43 1.6.4 Interaction of ToRSV with herbaceous plants ....................................... 46 1.7 Thesis objectives ............................................................................................. 49 Chapter 2: Temperature-dependent symptom recovery in Nicotiana benthamiana plants infected with ToRSV is associated with reduced translation of viral RNA2 and requires ARGONAUTE1 .................................................. 50 2.1 Introduction .................................................................................................... 50 2.2 Materials and methods ................................................................................... 51 2.2.1 Virus inoculations ................................................................................
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