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Analysis of Tomato Spotted Wilt Virus Effector-Triggered Immunity

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Analysis of Tomato Spotted Wilt Virus Effector-Triggered Immunity Analysis of Tomato spotted wilt virus effector-triggered immunity Dryas de Ronde Analysis of Tomato spotted wilt virus effector-triggered immunity Dryas de Ronde Thesis committee Promotor Prof. dr. J. M. Vlak Persoonlijk hoogleraar bij de leerstoelgroep Virologie, Wageningen University Co-promotor Dr. ir. R. Kormelink Universitair hoofddocent, leerstoelgroep Virologie, Wageningen University Thesis submitted in fulfilment of the requirements for the degree of doctor Other members at Wageningen University Prof. dr. F. Weber, University of Marburg, Germany by the authority of the Rector Magnificus, Dr. ing. F.L.W. Takken, University of Amsterdam Prof. dr. M.J. Kropff, Prof. dr. ir. B.P.H.J. Thomma, Wageningen University in the presence of the Dr. ir P. Maris, Dekker Chrysanten Thesis Committee appointed by the Academic Board to be defended in public This research was conducted under the auspices of the Graduate school of on Friday 8 November 2013 Experimental Plant Sciences. at 11 a.m. in the Aula Voor mijn ouders.............. “Charles Darwin had a big idea, arguably the most powerful idea ever. And like all the best ideas it is beguilingly simple” Richard Dawkins Dryas de Ronde Analysis of Tomato spotted wilt virus effector-triggered immunity 198 pages. Thesis Wageningen University, Wageningen, NL (2013) “Nobody said it was easy” With references, with summaries in Dutch and English The scientist ISBN 978-94-6173-721-2 Coldplay (2002) Table of contents Chapter 1: Dominant resistance against plant viruses: a review 1 Chapter 2 : Tsw-gene based resistance is triggered by a functional RNA 37 silencing suppressor protein of the Tomato spotted wilt virus Chapter 3: Analysis of Tomato spotted wilt virus NSs protein indicates 63 the importance of the N-terminal domain for avirulence and RNA silencing suppression Chapter 4: Analysis of a putative interaction between AGO1 and the 85 Tomato spotted wilt virus NSs protein Chapter 5: Identification and characterisation of a new class of 103 temperature-dependent Tomato spotted wilt virus resistance breaking isolates of Tsw-based resistance and the development of a diagnostic tool Chapter 6: General discussion 131 Appendices: References 142 List of abbreviations 166 Summary 171 Samenvatting 175 Dankwoord 179 About the author 185 List of Publications 187 EPS Educational certificate 188 Chapter 1 Dominant resistance against plant viruses: a review Chapter 1 Dominant resistance against plant viruses: a review Abstract While throughout the years reviews on resistance genes have appeared with regular intervals, these mostly had their main focus on fungal and bacterial To establish a successful infection plant viruses have to overcome a defence system resistance genes, primarily due to the large amount of data available. This chapter composed of several layers. This chapter will overview the various strategies aims to present an overview on the state of the art on resistance genes against 1 plants employ to combat viral infections with main emphasis and a state of the art plant viruses, with emphasis on single dominant resistance genes. Prior to this, a description on single dominant resistance (R)-genes against plant viruses and the brief introduction will be given on the versatile ways plants try to combat viruses to corresponding avirulence (Avr)-genes identified so far. The most common models prevent the establishment of an infection. to explain the mode of action of dominant R-genes will be presented. Finally, the The very basis of the fact that plant viruses cannot infect all plants is due to a hypersensitive response (HR) and extreme resistance (ER), both often triggered after mechanism called non-host resistance (NHR) (For an extensive review on this, see induction of dominant R-genes but not the cause for resistance, will be described. Uma et al. (2011)). NHR holds for all plant pathogens and is a generic, nonspecific In light of the scope of this thesis, the functional and structural similarity ofR -genes resistance against pathogens which is divided into two main types, distinguished of plants to sensors of innate immunity from animal cell systems will briefly be by the mechanism and mode of recognition (Mysore and Ryu, 2004). Type 1 is the described. most pre-dominant type of NHR and presents a basic defence mechanism that prevents pathogen invasion, e.g. thickening of the cell-wall, secondary metabolite production, etc. This type of resistance usually is symptomless. In contrast, type 2 I. Introduction NHR is associated with induction of necrosis at the site of infection, and is induced when pathogens overcome type 1 resistance. Here, the pathogen is recognised When looking around in nature, it is quite obvious to see that most plants are through specific structures or proteins that are associated with the pathogen. The healthy and do not seem to suffer from any serious infection. This can only be true if recognition of these structures/proteins, so called microbe associated molecular plants, like all other organisms, have an advanced defence system. In past decades, patterns (MAMPs) or PAMPS (Pathogen), takes place by pattern recognition scientists have shown that indeed plants have a unique and complex defence receptors (PRRs) on plant plasma membranes. These PRRs recognise conserved system that consists of several layers, which enables them to avoid, suppress or structures of pathogens, like flaggelin from the flagella of bacteria or chitin from the actively defend against pathogens from all kingdoms like fungi, bacteria, nematodes cell wall of fungi, and induce a so called PAMP triggered immunity (PTI) response and viruses. Of all plant viruses known, only a few cause serious diseases and, if (Jones and Dangl, 2006). so, mostly limited to a very small number of crops. In general, most viruses have a Since plant viruses need to overcome the physical barrier of a cell wall, they limited (natural) host range and the number of so-called non-hosts exceeds those enter their host cells either via mechanical inoculation or the infection is mediated of hosts. In those plants that are hosts, viruses encounter different mechanisms of by vectors like insects, nematodes or even fungi. Therefore, recognition by PRRs defence. Some plants act general against all viruses and this response is part of the on the plasma membrane does not apply here. One of the first innate immune innate immune system, while other plants are virus-specific hosts. In the latter case responses all plant viruses encounter when invading a host consists of antiviral resistance genes of the host are involved that leads to necrosis at the site of virus RNA silencing (also called RNA interference (RNAi) and in the very early days post- entry upon activation, and prevents further infection of the entire host plant. In transcriptional gene silencing (PTSG)). RNA silencing is a host response triggered several cases resistance genes do not confer absolute resistance against a virus and by double stranded (ds)RNA. These molecules thus act as a MAMP/PAMP and in low levels of virus replication can still be observed. In those cases the genes are also which RNAi can be regarded as PTI. The main difference with pathogens such as referred to as partial resistance genes or tolerance genes. fungi and bacteria is that recognition of viral MAMPs/PAMPs occur intracellularly 2 D. de Ronde 2013 3 Chapter 1 Dominant resistance against plant viruses: a review (Ding and Voinnet, 2007). genes. A very nice example of the latter case has recently been described with RNA silencing mainly consists of two major ‘branches’; the first one is that the cloning and characterisation of the Ty-1 resistance gene from tomato against of small-interfering (si)RNAs, and one of the hallmarks for antiviral RNAi, and Tomato yellow leaf curl geminivirus (TYLCV) (Verlaan et al., 2013). This gene encodes the second one is that of (host-gene encoded) micro (mi)RNAs involved in gene an RNA-dependent RNA polymerase (RdRp) that amplifies the RNAi signal, causing 1 regulation. MicroRNAs and siRNAs share structural and functional similarities, but enhanced methylation of the viral DNA genome (siRNA directed DNA methylation: differ by their biogenesis pathways. Although dsDNA viruses have also been shown RdDM) and thereby leading to transcriptional silencing of geminivirus genes. to encode miRNAs that are involved in the modulation of the hosts’ innate immune Tomato plants containing Ty-1 do not show symptoms upon challenge with TYLCV, responses, these will not be discussed here (for an extensive description of RNAi, but low levels of virus can still be detected (Verlaan, PhD-thesis 2013). see reviews on this by Ding (2010) and Sharma et al. (2012)). The antiviral RNAi Recessive resistance (Truniger and Aranda, 2009) so far has mainly been response is induced by viral double stranded (ds)RNA molecules that arise from described for viruses, and relies on the observation that viruses require host factors replicative intermediates or secondary RNA folding structures. These structures (also called susceptibility factors) to enable an infection. The inability of interaction are sensed by a host RNase type III-like enzyme called Dicer-like (DCL) protein and between such host factor and the virus leads to resistance. Since susceptibility cleaved into short interfering (si)RNA of 21-24 nucleotides (nt) in size (Sharma et al., factors are dominant, a resistance based on these requires all gene copies to be 2012). The siRNAs generated are unwound and only one strand, the so-called guide- in the (resistant) recessive state. This explains why such resistance is generally strand, is uploaded into a functional protein complex termed RNA-induced silencing termed recessive resistance. The majority of the recessive resistance genes known complex (RISC). This activated complex next surveils and subsequently degrades against plant viruses have been reported for potyviruses (Kang et al., 2005) and (viral) RNA target molecules with sequence complementarity to the guide-strand.
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