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Ilyas, R.;  Rohde, M.J.;  Richert-Pöggeler, K.R.;  Ziebell, H. Latent Infection by Tobamoviruses. Encyclopedia. Available online: https://encyclopedia.pub/entry/26873 (accessed on 27 July 2024).
Ilyas R,  Rohde MJ,  Richert-Pöggeler KR,  Ziebell H. Latent Infection by Tobamoviruses. Encyclopedia. Available at: https://encyclopedia.pub/entry/26873. Accessed July 27, 2024.
Ilyas, Rabia, Mareike J. Rohde, Katja R. Richert-Pöggeler, Heiko Ziebell. "Latent Infection by Tobamoviruses" Encyclopedia, https://encyclopedia.pub/entry/26873 (accessed July 27, 2024).
Ilyas, R.,  Rohde, M.J.,  Richert-Pöggeler, K.R., & Ziebell, H. (2022, September 05). Latent Infection by Tobamoviruses. In Encyclopedia. https://encyclopedia.pub/entry/26873
Ilyas, Rabia, et al. "Latent Infection by Tobamoviruses." Encyclopedia. Web. 05 September, 2022.
Latent Infection by Tobamoviruses
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This entry is adapted from the peer-reviewed paper 10.3390/plants11162166

Tobamoviruses are among the most well-studied plant viruses and yet there is still a lot to uncover about them. On one side of the spectrum, there are damage-causing members of this genus: such as the tobacco mosaic virus (TMV), tomato brown rugose fruit virus (ToBRFV) and cucumber green mottle mosaic virus (CGMMV), on the other side, there are members which cause latent infection in host plants. New technologies, such as high-throughput sequencing (HTS), have enabled people to discover viruses from asymptomatic plants, viruses in mixed infections where the disease etiology cannot be attributed to a single entity and more and more researchers a looking at non-crop plants to identify alternative virus reservoirs, leading to new virus discoveries. However, the diversity of these interactions in the virosphere and the involvement of multiple viruses in a single host is still relatively unclear. For such host–virus interactions in wild plants, symptoms are not always linked with the virus titer.

latent tobamoviruses asymptomatic infection host–virus interaction

1. Introduction

The genus Tobamovirus comprises positive-sense, single-stranded RNA (+ssRNA) viruses belonging to the family Virgaviridae and contains 37 recognized and several tentative species [1]. These viruses can infect a wide range of host plants, the type member tobacco mosaic virus (TMV) alone is known to infect approximately nine plant families and at least 125 individual plant species including tobacco, tomatoes, cucumbers and orchids [2].

2. Disease Symptoms

Tobamovirus disease symptoms can vary depending on the host plant, virus species and environmental conditions. Leaves of infected plants appear to be deformed, mottled or display a mosaic pattern [2]. Sometimes, in case of severe infection, systemic necrosis and defoliation occurs depending on biological (age of plant, cultivar, virus strain, etc.) and environmental factors (temperature, light intensity, etc.) [3]. TMV and tomato mosaic virus (ToMV) are the most extensively studied species and they commonly cause chlorosis, mosaic patterns and leaf distortion on susceptible hosts (Figure 1). Severe infections can also lead to systemic necrosis and defoliation. Pepper mild mottle virus (PMMoV) and tobacco mild green mosaic virus (TMGMV) infect vegetables in the family Solanaceae. PMMoV usually causes milder symptoms on leaves but is more severe on fruits causing a reduction in size and number, uneven ripening, corky or necrotic rings and internal necrosis. Tomato brown rugose fruit virus (ToBRFV) was first described by Salem et al. [4] and, since then, has become a threat in tomato growing regions of the world [5]. The symptoms appear both on leaves and on fruits causing deformation, yellowing and necrosis [6]. The leaves show interveinal yellowing and mosaic patterns while the fruits show marbling and discoloration, which reduces the market quality of the fruits [4][5][7].
Plants 11 02166 g001
Figure 1. (A) TMV symptoms on Nicotiana tabacum cv. ‘Samsum nn‘, showing leaf distortion, mosaic pattern and chlorosis; (B–D) ToBRFV symptoms on tomatoes showing mosaic pattern, leaf narrowing and rugose spots on fruits.
Apart from the agriculturally important crop plants, several new tobamoviruses have been detected infecting horticultural crops. Two tobamoviruses have been identified from hibiscus (Hibiscus latent Singapore virus (HLSV) and hibiscus latent fort pierce virus (HLFPV) [7][8]) Similarly, two tobamoviruses have been reported from wax flower plants belonging to Hoya spp. showing chlorotic ring spots and irregular leaf chlorosis. [9][10].

3. Genome Organization

Tobamoviruses are one of the most studied viruses due to their availability and ease of use in biotechnological studies [11]. A single virion of TMV is 18 nm wide and 300–310 nm long. The encapsidation of subgenomic RNA (sgRNA) results in shorter virions of 32–34 nm length, but these are a minor component of the total virion population [1]. The rod-shaped virions have an inner core of 4 nm diameter, which contains a +ssRNA molecule (Figure 2). The outer core is made up of 2100 subunits of coat protein. These subunits are arranged in the form of a right-handed helix around the RNA molecule [12]. Species demarcation criteria for tobamoviruses are based on nucleotide sequence similarity of the total genome. Less than ten percent difference in nucleotide sequence is defined to identify strains of a species [1].
Plants 11 02166 g002 550
Figure 2. Structural diagram of a TMV particle. Protein subunits are shown in purple while the ssRNA is shown in orange. Source: Image created in Biorender.
The extreme stability of tobamoviruses and their presence in the environment has been attributed to their structure [13]. TMV particles were found to be stable after heating for 30 min at 60 °C, at pH ranges between 2–10 and in organic solvents of up to 80% by volume. Particles lose their protein subunits from the 5′ terminal of RNA in alkaline solutions of pH 9 and above.
Purified TMV can be infectious even after 50 years of storage at 4 °C [13]. TMV has been persistently found in the environment including clouds, water, glacial ice and soil [14]. The persistence of tobamoviruses in water may contribute to their dissemination in the environment, as well as agricultural systems. Tobamoviruses have been detected in natural water bodies near and far from agricultural production in Europe and North-America [15].
The +ssRNA genome is approximately 6300 nt to 6800 nt in length. Figure 3 shows a schematic representation of the genome organization of TMV. Two overlapping ORFs begin at the 5′ proximal start codon. Termination at the first in-frame stop codon produces a 125–130 kDa protein. A 180–190 kDa protein is produced by read-through of its leaky termination codon approximately 5–10% of the time. These two proteins are required for replication and are produced from the genomic RNA. In addition, three more proteins are translated from two co-terminal sgRNAs of approximately 1.6 kb and 0.7 kb in length [16].
Plants 11 02166 g003
Figure 3. Schematic diagram of genome organization of TMV: ORFs encoding viral proteins are shown in blue. The 126 kDa replicase protein and the 183 kDa replicase read-through protein are translated from the genomic RNA (black), while the remaining proteins are expressed from separate subgenomic RNAs (gray). Image was modified from the NCBI Reference Sequence (NC_001367.1) [16] using CLC main workbench 21 and Inkscape 1.1.
The next ORF encodes the 28–34 kDa movement protein, which has RNA-binding activity and is required for cell-to-cell movement [17][18]. A positively charged protein was also found to be expressed from the MP-associated sgRNA [19]. This 4–8 kDa protein has been shown to increase the virulence in N. benthamiana and may be associated with cellular movement [20]. The 3′ proximal ORF encodes a 17–18 kDa coat protein (CP). A sgRNA containing an ORF for a 54kDa protein that encompasses the read-through domain of the 180–190 kDa ORF has been isolated from infected tissue, although no protein has been detected [12][21].
The 5′-UTR region of TMV starts with an m7G-capped G residue, which is followed by a ~70 nt G-deficient sequence, called an omega sequence (Ω), that contains multiple CAA repeats. The sg RNAs also contain these motifs [18]. Several tobamoviruses contain such CAA repeats in 5′-UTR [22]. The 3′-UTR in TMV RNA lacks a 3′poly-(A) tail and contains sequences that can be turned into a series of pseudoknot structures, followed by a tRNA-like terminus (Figure 4). This addition of 204 nt in 3′-UTR stabilizes the mRNA and enhances translation [22]. These UTR regions play multiple roles in translation and replication of tobamoviruses. Recently, 2 tobamoviruses from hibiscus have been reported to contain an internal 3′-poly(A) tail region [8][23][24][25] raising questions about functions and diversity of UTRs in tobamoviruses.
Plants 11 02166 g004
Figure 4. Schematic diagram of 3′-UTR of TMV RNA. Translational stop codon is underlined and nt numbers from the 3′ region are indicated. Image source [22].

4. Transmission

The spread of tobamoviruses is mainly driven by mechanical transmission. Seed transmission is also possible. Tobamoviruses do not infect the embryo but can be transmitted to the seedling from the surrounding tissue during germination. Tobamoviruses can be found in the seed coat and sometimes in the endosperm [26]. Seed transmission from outside of the embryo requires a high stability of the viral particles and does not occur at a high rate [27]. However, seed transmission is an important factor in the dissemination of tobamoviruses such as ToBRFV.
Other sources of primary inoculum include the juice of infected fruits, as well as plants grown in infected soil or grafted with infected material [28]. Bumblebees, which are commonly used for pollination in tomato crops, have also been shown to carry ToBRFV particles and hives from affected greenhouses can introduce the virus into new facilities [28].

5. Symptoms—To Be Seen or Not to Be Seen: The Concept of Viral Latency and Asymptomatic Infection

As a part of the disease triangle, host, virus, and environment equally play a role in disease establishment. Therefore, the viral symptoms are dependent on the right host and a suitable environment. Over the last few decades, there have been various meanings and explanations for asymptomatic infection and virus latency. This terminology is loosely used in the context of a host–virus interaction that does not give rise to visible disease symptoms. Roger Hull explains latency as a consequence of tolerance: where virus is able to replicate and move systemically in the host with little or no impact on the plant’s overall health [29]. On the other side, Takahashi et. al. defines latency as a phenomenon when the virus is in a dormant state and does not replicate in the host [30]. They discuss that the asymptomatic infection can either result from tolerance or persistence.

6. Mechanisms That May Explain Latent/Asymptomatic Infection

The existence of several definitions of latent infection gives rise to even more explanations of mechanisms that may cause this phenomenon. According to Roger Hull [29], there can be six possible reasons for an asymptomatic infection:

(1) Infection with a very mild virus strain,

(2) A tolerant host plant,

(3) Leaves that escape infection because of their age and position on the plant,

(4)‘Recovery’ from the disease symptoms in newly formed leaves,

(5) Dark green areas in a mosaic pattern,

(6) Plants that are infected with cryptic viruses.

Viral populations encompass different genetic variants, and their distribution is shaped by selection and genetic drift. In addition to virus replication and maintenance, properties of the host plant play an important role for the selection of viruses. This includes the adaptation to plant resistance, plant defense mechanisms and also the relationship between virus replication and plant fitness. An interesting aspect of viral genome organization are the multifunctional proteins and overlapping open reading frames. This results in a trade-off regarding selection for different functionalities. Although RNA viruses can show high mutation rates, their proteins are not more variable than those of DNA-viruses [31][32]. An independent assessment of mutation rates without the influence of selection is difficult. A mutation rate of 0.02–0.05, with multiple mutations in 35% of cases and 69% of indels was found in the mutational spectrum [33]. The recombination of RNA viruses is also an important source of genetic variation and has been shown to occur in tobamoviruses in the case of TMV and ToMV [34].
Genetic variation can lead to differences of symptom severity in plants infected with different strains. For example, it has long been known that attenuated strains of TMV exist, which cause little or no symptoms in tobacco plants and may even interfere with the development of symptoms in a mixed infection with a more severe strain [35][36]. In some cases, changes in symptom severity could be associated with specific mutations. For example, recovery mutants of the mild strain TMV-K were used to pinpoint nonsense mutations in the replicase and movement protein [37], similar mutants are known for other tobamoviruses [38][39]. On the other hand, mutations can also lead to increased virus reproduction and/or symptom development. An example is an increase of TMV replication due to disruptions in its the secondary structure [40]. Since the expression of sub-genomic viral RNA is regulated by sub-genomic promoter and enhancer elements, disruption of the relevant motifs also leads to changes in protein expression [41]. These regions might also be targets of alleviating mutations.
Most studies on tobamoviruses focus on virus multiplication as the criteria for trade-off between host–virus interactions. However, when it comes to host range determination, there are two important components of viral fitness: particle stability and infectivity [42]. As shown by a series of studies, maintaining the three-dimensional structure of TMV CP was essential for N-gene resistance elicitation [43]. Therefore, resistance breaking is associated with altered particle stability. A trade-off between increased viral reproduction and extended survival can lead to slower rates of replication for enhanced particle stability [42]. Fraile et al. explain infectivity as the relationship between inoculum dose and infection success [42]. Mutational analysis experiments from Culver et al. showed increased particle stability correlated with decrease in infectivity and less efficient viral translation [44].
Another reason that might explain latency can be the balance between host defense and viral counter defense. Tobamoviruses have co-evolved with their hosts [45] and have developed sophisticated mechanisms to counteract the host defense systems. It might be possible that these finely tuned interactions allow some tobamoviruses to persist in hosts without causing much damage. Naturally occurring latent tobamoviruses have not been studied extensively. There are studies on TMV that support the idea that plant viruses can suppress host defense signaling by promoting the degradation of ATF2, a plant NAC transcription factor, which regulates the expression of PTI-responsive genes [46].
The beneficial interaction between plant viruses and hosts have been discussed in more detail in previous studies [47][48]. Experimental evidence supports the beneficial impact of accommodating long-term virus infection, especially in natural environments [48]. TMV infection has shown to improve the plant resilience in sub-optimal environmental conditions, for example, tolerance to drought [49]. Virus-induced drought tolerance is associated with global reprogramming of plant gene expression, changes in hormone signaling and increased accumulation of metabolites and antioxidants [20]. Interestingly, recent studies suggested that the benefits of increased drought resistance can be offset by increased virus virulence [20]. Maintaining persistent virus infection can also improve the plant resistance to biotic stress including non-vector herbivory insects, other viruses or unrelated pathogens [48][50].

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Subjects: Virology; Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Rabia Ilyas
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Mareike J. Rohde
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Katja R. Richert-Pöggeler
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Heiko Ziebell
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