Baculovirus-Induced Insect Behaviour: From

Baculovirus-Induced Insect Behaviour: From

Baculovirus-induced insect behaviour: from genes to brains genes to from insect behaviour: Baculovirus-induced Baculovirus-induced Invitati on insect behaviour: from genes to brains You are cordially invited to attend the public defense of my PhD thesis enti tled: Baculovirus-induced insect behaviour: from genes to brains On Friday, 31th August at 16:00 p.m. in the Aula of Wageningen University, Generaal Foulkesweg 1, Wageningen Yue Han [email protected] Yue Han Paranymphs Yuxi Deng [email protected] Corien Voorburg [email protected] 2018 Yue Han Baculovirus-induced insect behaviour: from genes to brains Yue Han Thesis committee Promotor Prof. Dr M.M. van Oers Professor of Virology Wageningen University & Research Co-promotor Dr V.I.D. Ros Assistant professor, Laboratory of Virology Wageningen University & Research Other members Prof. Dr L.E.M. Vet, Wageningen University & Research Prof. Dr J.A. Jehle, Julius Kühn Institute, Darmstadt, Germany Prof. Dr A.T. Groot, University of Amsterdam Dr R.P. van Rij, Radboud University Medical Center, Nijmegen This research was conducted under the auspices of the Graduate School for Production Ecology and Resource Conservation. Baculovirus-induced insect behaviour: from genes to brains Yue Han Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday August 31, 2018 at 4 p.m. in the Aula. Yue Han Baculovirus-induced insect behaviour: from genes to brains, 190 pages. PhD thesis, Wageningen University, Wageningen, the Netherlands (2018) With references, with summary in English ISBN: 978-94-6343-467-6 DOI: https://doi.org/10.18174/454937 Table of Contents Chapter 1 General introduction 1 Chapter 2 Virus induced behavioural changes in insects 15 Chapter 3 Parasitic manipulation of host behaviour: baculovirus SeMNPV 39 EGT facilitates tree-top disease in Spodoptera exigua larvae by extending the time to death Chapter 4 Timely trigger of caterpillar zombie behaviour: temporal 63 requirments for light in baculovirus-induced tree-top disease Chapter 5 Baculovirus PTP2 functions as a pro-apoptotic protein 77 Chapter 6 Substrate identification of baculovirus protein tyrosine phosphatase 101 Chapter 7 Baculovirus invasion of the lepidopteran central nervous system 127 Chapter 8 General discussion 147 References 161 Summary 177 List of Publication 180 About the Author 181 Acknowledgements 182 Ceritficate 188 Chapter 1 General introduction and thesis outline 1 2 Chapter 1 General introduction and thesis outline Parasites and the extended phenotype The word ‘parasite’ is originally derived from the Greek term “parasitos”, which was used to describe persons tasting food at the tables of noble families in order to check whether the food was poisoned or safe (Etymonline.com, 2017). Therefore, these “parasitos” were nourished without working and lived at the expenses of others. Later the use of this term was changed to describe organisms that live on the expense of others, and as such obtain their food from other animals or plants that are commonly called the host of the parasite (Long and Staskawicz, 1993; Mehlhorn, 2015). During billions of years of evolution, parasites and hosts have developed complex mutual relationships and it is known that parasites affect many aspects of their hosts, including metabolism, physiology, development, morphology, and behaviour (Tully and Nolan, 2002; van Houte et al., 2013). As compulsory intracellular parasites, viruses are also known to affect many aspects of their hosts (Mehlhorn, 2015; Poulin, 2000; van Houte et al., 2013). In the famous book “The Selfish Gene” published in 1976, Richard Dawkins presented his “gene-centred view of evolution” theory. According to his theory, the basic unit of evolution is the individual gene instead of the individual organism or groups of similar organisms. Therefore, a gene is expected to maximize the number of copies of its own and to pass them on to the next generation (Dawkins, 1976). In the book “The Extended Phenotype” published in 1982, Richard Dawkins further expanded his evolutionary theory and introduced the concept “the extended phenotype”. He proposed that the phenotype should not be limited to biological processes (such as protein synthesis, tissue growth), but should also include all the effects that a gene has on its environment. There are three forms of extended phenotypes: the first is the ability of animals to modify their environment using architectural constructions, such as dam-making behaviour of beavers. The second form is the ability to manipulate other organisms, also referred to as “parasitic manipulation”. In this form, the observed host phenotype is a consequence of the expression of the parasite’s genes. Famous examples include the suicidal behaviour of crickets infested by hairworms (Thomas et al., 2002) and the zombie behaviour of carpenter ants infected by fungi (Hughes et al., 2011). In this thesis, I will look into the behavioural and physiological phenotypes of caterpillars infected by baculoviruses (as further detailed below) and I will study how the expression of viral genes is affecting the observed host phenotypic behaviour. The third form of an extended phenotype includes the action at a distance of a parasite on its host, such as the behavioural manipulation by egg-laying female cuckoos, impelling other birds to feed the cuckoo chicks (Dawkins, 1982). 3 Chapter 1 General introduction and thesis outline Baculoviruses The family Baculoviridae is a group of arthropod-specific viruses with double stranded, circular genomes ranging from 80 to 180 kbp (van Oers and Vlak, 2007). Baculoviruses have been reported to infect more than 700 insect species belonging to the orders Lepidoptera, Diptera and Hymenoptera (Slack and Arif, 2007). Baculovirus genomes contain roughly 90 to 180 open reading frames (ORFs) (van Oers and Vlak, 2007). Two different types of virions, which are morphologically different but genetically identical, are produced during infection. Budded viruses (BVs) are responsible for systemic infection within the host and occlusion derived viruses (ODVs) are responsible for primary infection of the host’s epithelial midgut cells. BVs consist of a single, enveloped nucleocapsid and obtain their envelope from the plasma membrane of infected cells. In contrast, ODVs may contain single or multiple nucleocapsids within a single envelope and ODVs obtain their envelope from the inner nuclear membrane of the infected cells. ODVs are embedded in a paracrystalline proteinaceous matrix, forming an occlusion body (OB). OBs are extremely stable and protect virions from harsh conditions (Slack and Arif, 2007). Based on the morphology of OBs, baculoviruses are named nucleopolyhedroviruses (NPVs) or granuloviruses (GVs) (Rohrmann, 2013b). NPVs and GVs differ in the protein that forms the paracrystalline matrix: polyhedrin for NPVs and granulin for GVs. According to the number of nucleocapsids within each ODV, NPVs can be further divided into multiple nucleopolyhedroviruses (MNPV) and single nucleopolyhedroviruses (SNPV). Taxonomically, baculoviruses are divided into four genera: Alphabaculovirus (lepidopteran- specific NPVs), Betabaculovirus (lepidopteran-specific GVs), Gammabaculovirus (hymenop teran-specific NPVs) and Deltabaculovirus (dipteran-specific NPVs) (Jehle et al., 2006). Based on phylogenetic analyses, the Alphabaculovirus genus is further divided into Group I and Group II NPVs (Zanotto et al., 1993). Group I NPVs use the GP64 protein as BV envelope fusion protein, whereas Group II NPVs and beta- and deltabaculoviruses use the F protein as the BV envelope fusion protein (Rohrmann, 2013b; Slack and Arif, 2007). Gammabaculoviruses do not have the BV phenotype and as a consequence are limited to the gut (Lucarotti et al., 2012). The baculovirus infection cycle starts with ingestion of virus-contaminated food by insect hosts. OBs migrate together with food into the insect’s midgut (Figure 1, Step A). Under the alkaline conditions (pH 9-11) in the insect midgut, the OBs dissolve thereby releasing the occluded ODVs (Figure 1, Step A). Subsequently, ODVs travel through the peritrophic membrane, a network of proteins and chitin that protects the midgut epithelium (Hegedus et al., 2009). ODVs then bind and fuse with the microvilli of the midgut epithelium cells (more in particular the 4 Chapter 1 General introduction and thesis outline columnar cells) and start the first round of infection (Figure 1, step B) (Rohrmann, 2013a). After the first round of virus replication in the nucleus of the infected midgut cells BVs are produced (Figure 1, step B and C). These BVs then infect adjacent tissues or are transported to other tissues via the hemolymph and trachea, causing a systemic infection (Figure 1, step B and C) (Rohrmann, 2013a). Consequently, more BVs are produced from newly infected cells. In the late stage of infection, ODVs are produced in the nucleus of infected cells and packed into OBs (Figure 1, step C). After the insect has succumbed to the infection, viral enzymes such as chitinase and cathepsin (Rohrmann, 2013a) liquefy the cadaver, releasing OBs into the environment (Figure 1, Step D). OBs are produced in large numbers, and virus yields up to 108 OBs per caterpillar have been reported for alphabaculoviruses (Rohrmann, 2013a). Figure 1. Baculovirus infection cycle (Rohrmann,

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