Abstract
Lycopersicum esculentum (tomato), is a member of the Solanaceae family with a global production of approximately 159 million tons per year. However, the productivity of tomato is constrained by many factors including biotic and abiotic stresses. Of these, tomato spotted wilt virus (TSWV) is one of the major threats to tomato productivity. TSWV is a ribovirus and is transmitted by small insects commonly known as thrips. Several approaches have been utilized in the past few decades to understand the plant and thrips responses against TSWV. These include conventional molecular biology to high-throughput genomics, transcriptomics, and proteomics approaches which have led to the identification of several genes/proteins involved in the tomato/thrips-TSWV interaction. Moreover, several genes (such as Sw-1a and Sw-1b, sw-2, sw-3, sw-4, Sw-5, Sw-6, and Sw-7) and proteins (like DNA-J) have also been identified from its plant hosts which provide resistance against this deadly virus. In this mini-review, we are summarizing the progress made so far in this area to provide the overview of tomato, thrips and TSWV interaction.
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Introduction
Tospoviruses (Order Bunyavirales, family Tospoviridae) are one of the major threats to crop productivity resulting in the loss of over $1 billion worldwide (Prins and Goldbach 1998). Among these tospoviruses, tomato spotted wilt virus (TSWV) is one of the deadliest viruses with a host range of more than 1000 plant species belonging to more than 85 families including tomato, bean, lettuce, groundnut, pepper, potato, and tobacco, among others. Tomato spilt disease was first identified in 1915 in Australia, however, it was only 1930, when this particular virus was identified as the causative agent of this disease (Oliver and Whitfield 2016). TSWV is spread through small insects, Frankliniella occidentalis, commonly known as western flower thrips that act as a vector of this virus. Moreover, tospoviruses also replicate in their thrips vectors, thus the insects not only spread the virus but also serve as another virus host. Thrips acquire the virus during their larval stages from infected plants and transfer these to the healthy plants at the end of their larval stages (Fig. 1a). As per the ‘Food and Agriculture Organization (FAO)’, the tomato is the 9th most cultivated agricultural crop with an annual production of 159 million tons per year (Ghatak et al. 2017) and thus, the economic loss because of the TSWV on just the tomato plants can be expected. A case study where the effect of TSWV on tomato yield was studied from May to November in Samsun province of Turkey, showed that the TSWV caused 42.1 and 95.5% reduction in yield and marketable value of tomato, respectively (Sevik and Arli-Sokmen 2012). Because of a wide host range of TSWV, similar economic loss has been reported in other host plants, especially in peppers (Ramchiary et al. 2014).
Tremendous efforts have been given in the past to control this deadly virus. However, conventional practices to control this virus remained futile because of the several factors including large amount of inoculum available in the field; variability of the isolates, short virus acquisition period, its multiplication in the vector, high transmission efficiency, the wide distribution of the thrips and their resistance to many insecticides (Roselló et al. 1998). Therefore, development of genetically resistant tomato cultivars is the need of the hour for managing this particular virus and this deadly disease.
Biology of TSWV
TSWV virions are roughly spherical in shape with a diameter of 80–120 nm. The outer membrane is made up of lipoproteins, containing two, GN and GC, glycoproteins (where N and C represent amino and carboxy-terminal, respectively), which play crucial roles in the particle assembly, maturation, and release in the host organism (Nagata et al. 2000). Recently, the 3-D structures of these two proteins were predicted using computational docking experiments which showed that the carboxy-terminal of GN is necessary for heterodimerization with GC. Moreover, a protein–ligand docking study predicted tunicamycin and distamycin-A as most efficient drugs against TSWV (Soundararajan et al. 2015).
As of today, complete genome sequence of several TSWV isolates including Brazilian TSWV BR-01 from Nicotiana rustica (De Haan et al. 1990; de Haan et al. 1991; Kormelink et al. 1992), TSWV-YN from from Chenopodium quinoa (Hu et al. 2011), TSWV-KP from Capsicum annuum (Kim et al. 2013) and TSWV-1, TSWV-2 and TSWV-3 from tomato and pepper (Lee et al. 2011) have been reported. A comparative analysis has shown more than 90% nucleotide sequence identity in the genome sequence of these TSWV isolates, indicating a relatively conserved genome of this virus (Hu et al. 2011; Lee et al. 2011). Moreover, a comparative genome analysis of three Spanish isolates, LL-N.05 (wild type), Pujol1TL3 (Sw-5 resistance breaking) and PVR (Tsw resistance breaking) was also carried out (Debreczeni et al. 2015).
In general, TSWV genome is composed of ribonucleoproteins carrying three different genomic RNAs with a negative strand genomic RNA of ~ 8.9 kb (large) and two ambisense RNAs of ~ 4.8 kb (medium) and ~ 2.9 kb (small) (Turina et al. 2016). As the polarity of the large RNA is negative, it has to be copied to complementary strand before it can be read (Kim et al. 2013). This complementary strand of large RNA contains a single ORF which encodes for a 331.5 kDa RNA-dependent RNA polymerase that assists in RNA replication (Van Poelwijk et al. 1996; Kim et al. 2013). The medium RNA encodes for a single polyprotein which is a precursor for both GN and GC glycoproteins. Later, this polyprotein is proteolytically digested to yield the mature GN and GC proteins of 58 and 95 kDa, respectively (Whitfield et al. 2008). The small RNA encodes for a 28.8 kDa nucleocapsid protein (N). In addition to these, the medium and small RNAs also encode for two non-structural proteins of 33.6 and 30 kDa which are named as NSM and NSS, respectively, by an ambisense coding strategy (Lovato et al. 2008; Guo et al. 2017). These proteins are called non-structural proteins as these are not found in the assembled virions and only present in the TSWV-infected cells (Ullman et al. 1993). The NSM protein facilitates the spread of the virus throughout the host, while the NSS protein is involved in the suppression of TSWV gene silencing (Lovato et al. 2008). All of these protein functions in a highly coordinated manner which helps in the successful establishment of the TSWV infection inside the host cells. It was reported that the proper and correct interaction between the NSM and N is required for the cell to cell transport of the virus through plasmodesmata (Kormelink et al. 1994). Recently, the crystal structure of N was produced, showing that N features a body domain consisting of an N- and C-lobe with a positively charged groove and a potential RNA-binding site. Moreover, the body domains of N were found to be flanked by N- and C-terminal arms, mediating homotypic interactions to the neighboring subunits (Guo et al. 2017).
Replication of TSWV inside the thrips
Infection and replication of TSWV inside the thrips is a complex process and is governed by multiple interactions between virus and host proteins. During its journey from midgut to salivary glands, TSWV has to cross at least six membrane barriers inside the thrips (Whitfield et al. 2008). Midgut lumen of the thrips is the first check point where initial interaction between the TSWV glycoproteins and midgut receptors take place after which virus enters the host midgut cells probably by endocytotic pathway (Whitfield et al. 2008). Inside the midgut cells, virus is propagated to the adjacent midgut cells and also acquired by the larval thrips. From midgut cells, virus moves to the visceral muscle cells and primary salivary glands where it replicates. This whole cycle of virus multiplication inside the thrips starts from the virus acquisition by thrips at their larval stages (L1 and L2), virus persistence in the pupal stages (P1 and P2), and accumulation in the salivary glands (Nagata et al. 2002; Schneweis et al. 2017).
Glycoproteins play a major role in this whole life cycle of virus inside the thrips. It was shown that the mutations in the ORF of glycoprotein results in the loss of transmissibility of TSWV by thrips (Nagata et al. 2000; Sin et al. 2005). A specific nonsynonymous mutation in the glycoprotein ORF was found to inhibit the thrips transmissibility, however, it did not affect the virion assembly (Sin et al. 2005). In contrast, loss of thrips transmissibility because of the deletion mutations in the glycoprotreins’ ORF, also affected virus envelop formation (Nagata et al. 2000).
In vivo binding assays showed that a soluble form of TSWV glycoprotein GN binds to the epithelial cells of the midguts of larval thrips and decreases the TSWV acquisition, indicating that the GN may act as a viral ligand that mediates attachment of TSWV to receptors on the thrips midgut (Whitfield et al. 2004). Moreover, it was observed that feeding GN to the thrips results in a significant reduction in virus transmission, suggesting that the TSWV transmission by thrips can be reduced by exogenous application of viral glycoprotein (Whitfield et al. 2008). In addition to the glycoproteins, the involvement of NSs protein in the thrips transmissibility was also shown (Margaria et al. 2014). It was observed that TSWV carrying truncated NSs protein could not be transmitted by thrips, indicating a crucial role of NSs protein in TSWV transmission by thrips (Margaria et al. 2014).
Identification of TSWV-responsive genes/proteins in thrips
RNA-Seq is a powerful tool for the identification of differentially expressed transcripts during host–pathogen interaction. Therefore, several RNA-Seq-based transcriptome analysis has been carried out to identify the differentially expressed genes in western flower thrips in response to TSWV infection (Zhang et al. 2013; Schneweis et al. 2017; Shrestha et al. 2017). The very first study led to the identification of 36,339 unigenes of which 278 were related to the insecticide resistance (Zhang et al. 2013). Analysis of differentially expressed genes between the non-infected and infected thrips showed that the virus can regulate the cellular process and immune response in thrips, which might lead to low virus titers in thrips cells (Zhang et al. 2013). Moreover, an RNA-Seq-based whole-body transcriptome analysis of thrips was also carried out in response to TSWV infection at different developmental stages including first-instar larval (L1), pre-pupal (P1) and adult thrips (Schneweis et al. 2017). A total of 178, 181, and 127 genes were found to be differentially modulated in response to TSWV infection at L1-21 h, P1, and Adult-24 h developmental stage times, respectively. Functional annotation of these differentially expressed genes showed that these were majorly related to the host defense, insect cuticle structure, and development, metabolism and transport. Furthermore, a varied response to the TSWV infection was observed at different developmental stages, indicating a coordination between development and the virus dissemination route (Schneweis et al. 2017).
Along with the transcriptome analysis, proteomic analysis has also been carried out to identify the TSWV-responsive proteins in thrips (Badillo-Vargas et al. 2012). To increase the number of protein identification, authors first generated a partial thrips transcriptome database using 454-Titanium sequencing of cDNA generated after infection to TSWV. Using this database, a total of 37 differential proteins were identified between infected and non-infected larvae samples which were majorly associated with the infection cycle of another plant- and animal-infecting viruses and antiviral defense responses. In particular, proteins related to the cellular transport, cytoskeleton and cellular structure were differentially modulated, indicating that TSWV infection could lead to the disruption of cellular trafficking in thrips (Badillo-Vargas et al. 2012). Recently, another proteomic study was carried out to identify the defense-responsive proteins in thrips larvae in response to TSWV infection (Ogada et al. 2017). Using two-dimensional gel electrophoresis, 30 TSWV-modulated proteins were identified of which 22 and 8 showed increased and decreased abundances, respectively. Functional annotation of the TSWV-induced proteins showed that these were majorly involved in translation (26%), insect defense response (15%), signalling (13%), anatomical development (13%), cellular lipid metabolic processes (9%), 8% were structural proteins, 8% were linked to stress response, 5% in nucleotide metabolism and 3% were actin binding. The key proteins identified included 70 kDa heat-shock proteins, ubiquitin, and dermcidin, suggesting a responsive pattern of the vector’s innate immune system to viral infection (Ogada et al. 2017).
TSWV–tomato interaction
RNA silencing plays pivotal roles in gene regulation and defense against invading pathogens. Therefore, attempts were made to understand the RNA-silencing mechanism in tomato and tobacco during TSWV infection (Mitter et al. 2013; Ramesh et al. 2017). Viral small interfering RNAs (vsiRNAs) are virus-secreted RNAs that direct the RNA-silencing machinery of the plants which in turn targets the viral double-stranded RNA (dsRNA). Therefore, vsiRNAs were first characterized by deep sequencing in TSWV-infected tobacco and -tomato plants (Mitter et al. 2013). This study demonstrated that the total sRNA reads in TSWV-infected tomato were of 21, 22 and 24 nt, whereas N. benthamiana showed majorly 24 nt total sRNAs. Although, the detected vsiRNA reads were much higher in tomato as compared to N. benthamiana, the profile of vsiRNAs in terms of relative abundance of 21, 22 and 24 nt class size was found to be similar in both the hosts (Mitter et al. 2013). Another similar study used a transcriptomic approach to analyze the TSWV secreted vsiRNAs induced changes in the transcriptome of tomato (Ramesh et al. 2017). This study led to the identification of 2450 unique vsiRNAs that can potentially cross-react with the tomato transcripts majorly involved in basal cellular activities including enzymes, transcription factors, membrane transporters, and cytoskeletal proteins.
An NMR-based metabolomics study was carried out to investigate the host-plant resistance to thrips in wild and domesticated tomatoes (Mirnezhad et al. 2010). Thrips bioassays revealed that the wild and domesticated tomatoes exhibited different levels of thrips resistance and only wild tomatoes, particularly Solanum pennellii and S. habrochaites were found to be thrips resistant and showed lowest thrips damage. NMR profiles showed significant differences in the metabolites of resistant and susceptible tomatoes with the identification of acylsugars as a potential resistance factor for thrips in tomato (Mirnezhad et al. 2010). However, further follow-up experiments showed that very high concentrations of acylsugars and sesquiterpenic carboxylic acids are required for providing resistance against the thrips and thus these play only a minor role in tomato protection against these insects. These follow-up experiments led to the identification of methylketones, exhibiting a dose-dependent effect on thrips mortality (Unpublished data). Moreover, a previous study demonstrated that the low concentrations of total aromatic amino compared to total foliar protein were correlated with a decrease in damage by the thrips (Mollema and Cole 1996).
Efforts were also made to generate the transgenic plants showing resistance against TSWV infection. Transgenic (NahG) tomato plants overexpressing a salicylate hydroxylase gene from Pseudomonas putida showed early and dramatic disease phenotype after TSWV infection as compared to the wild-type (López-Gresa et al. 2016). Salicylate hydroxylase metabolizes salicylic acid (SA) to catechol and thus NahG plants cannot accumulate SA. Therefore, the development of unusual disease phenotype after TSWV infection in transgenic plants indicate a role of SA in basal resistance against TSWV. Application of acibenzolar-S-methyl, which is involved in the activation of systemic acquired resistance downstream of SA signaling, improves the resistance of transgenic tomato plants to TSWV infection, further suggesting the involvement of SA in disease resistance (López-Gresa et al. 2016). To investigate the protein-level differences between the genetically modified (GM) and non-GM plants, a proteomic study was employed in the early 2000s. Non-GM plants were developed by crossing L276 × RT (two parental lines), while the GM plants were developed by crossing L276–30.46 (L276 line containing nucleoprotein gene of TSWV and nptII genes) × RT (Corpillo et al. 2004). Results of this study showed no significant differences in the protein profiles between the genetically modified tomato plants, indicating that abundance of major proteins remain largely unchanged by the genetic manipulation and can be considered safe for human consumption, similar to the wild-type (Corpillo et al. 2004). However, further experimentations are required to validate this observation as this study utilized a gel-based proteomic approach which has limitations in detection and quantification of low-abundance proteins (Gupta et al. 2015) (Table 1).
Conclusions and future perspective
Development of TSWV-resistant plants is required to control TSWV-induced crop loss. However, for the development of GM tomato plants with higher resistance, it is important to first understand the mechanism of tomato and TSWV interaction. Research in the last few decades has increased our understanding of TSWV pathogenicity as well as tomato resistance against this virus. Several genes including five dominant and allelic (Sw-1a, Sw-1b, Sw-5, Sw-6, and Sw-7) and three recessive (sw-2, sw-3 and sw-4) genes involved in resistance to TSWV were previously identified from L. esculentum and L. pimpinellifolium (Lin et al. 2007; Saidi and Warade 2008). However, this resistance was found to be the strain-specific and quickly overcome by the virus, thus could not be utilized successfully in the breeding programs (Finlay 1953; Roselló et al. 1998). Moreover, the involvement of tomato-secreted DNA-J protein homologs were also reported in tomato–TSWV interaction (Soellick et al. 2000). DNA-J protein of tobacco and Arabidopsis has been shown to interact the movement proteins of TSWV which facilitates the cell to cell movement of the non-enveloped ribonucleocapsid structures and thus inhibition of the movement proteins can inhibit the spread of virus inside the host (Soellick et al. 2000). However, because of the tripartite genome organization, TSWV can undergo recombination with closely related viruses to generate genome heterogeneity, resulting in their rapid evolution (Qiu et al. 1998), making it difficult to control.
Advancement in technologies such as the development of RNA-Seq and mass spectrometers with improved sensitivity, has led to a boom in the scientific world in terms of identification of differentially expressed genes, proteins, and metabolites in response to different environmental cues. Therefore, future efforts should be given on the utilization of these high-throughput techniques for the identification of TSWV-induced genes/proteins in tomato and thrips (Fig. 1b). Identification of more TSWV-responsive genes/proteins would provide a better resource for crop improvement and development of TSWV-resistant thrips and tomato cultivars. Moreover, an integrated omics approach, utilizing transcriptomics, proteomics and metabolomics approach would provide even a better view of the TSWV responses in tomato and thrips. However, integrated studies always show a lack of correlation between the transcripts and protein expressions, because of the occurrence of several post-transcriptional and post-translational modifications. Translatome is relatively a newer field of research where translating mRNAs are isolated and are sequenced by cDNA microarray or RNA-Seq. As, in this approach, only translating mRNAs are sequenced, this technique provides a better correlation with the proteome profiling than transcriptome–proteome profiling. Utilization of these techniques, in future, will definitely help us understand the complex mechanism of TSWV-thrips/tomato interaction which is required for the generation of TSWV-resistant tomatoes.
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Acknowledgements
This work was supported by the National Research Foundation of Korea (NRF) Grant funded by the Korean government (NRF-2017R1A2B2009171), Basic Science Research Program through the NRF funded by the Ministry of Education, Science and Technology (NRF-2016H1D3A1937706) and the KRIBB Research Initiative Program.
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Gupta, R., Kwon, SY. & Kim, S.T. An insight into the tomato spotted wilt virus (TSWV), tomato and thrips interaction. Plant Biotechnol Rep 12, 157–163 (2018). https://doi.org/10.1007/s11816-018-0483-x
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DOI: https://doi.org/10.1007/s11816-018-0483-x