A Review on Ecology of Interactions in Soybean Vein Necrosis Orthotospovirus (SVNV): Plants, Vectors, Virus Dispersal and Management Perspectives

*Asifa Hameed, Cristina Rosa and Edwin G. Rajotte*

## **Abstract**

Soybean vein necrosis orthotospovirus (SVNV, Genus: *Orthotospovirus*, Family: *Tospoviridae,* Order *Bunyavirales*) is a vector and seed transmitted virus that infects soybean in different countries around the world. The purpose of this review paper was to provide information about SVNV, its geographic dispersal, vectors, disease transmission mode, alternative host plants, diagnostic tools and management. SVNV is a negative-sense single-stranded RNA virus reported in all soybean growing states in the USA, Egypt and Canada. SVNV can replicate in plants belonging to six different families, including the Leguminosae member mung bean, which is a major component of the diet of poor people of Asia. The most efficient and abundant SVNV vector species is *Neohydatothrips variabilis* (Beach.) (Sericothripinae: Thripidae). Five other insect species have the potential to transmit the virus, but their rate of transmission is very low. In addition to leaf necrosis, this virus can decrease seed oil content by 0.1% that may lead to a decrease in quality of SVNV infected seed in oilseed markets. In fact, in the infected seeds the quantity of the undesirable linolenic acid, a polyunsaturated fatty acid is increased. Broad presence of SVNV in all soybean growing regions points to the need to manage vector and virus. However, research is needed to determine various management options for the virus and vector including breeding for genetic resistance.

**Keywords:** soybean, soybean vein necrosis orthotospovirus, soybean thrips, symptoms, alternative hosts

## **1. Introduction**

Soybean is one of the most valuable oil seed, food, forage, biodiesel, feed, and leguminous nitrogen fixer crop which improves soil structure through nodule formation, nitrogen fixation and enhances farmer income along with multiple other benefits [1–4]. Soybean is the second most important broad acre agricultural crop in the US providing high cash benefits to farmers [5]. Soybean was first introduced

in the US for agricultural usage as a forage crop in 1804 [6], probably as part of an interchange of seeds between France and US. However, there is some evidence from Georgia which documents soybean cultivation in 1765. Since 1940, the area under soybean cultivation increased so much that it is now mainly used as an oil seed crop. The expansion of soybean cultivation increased from about 2.7 billion bushels in 2000 to 4.39 billion bushels in 2017 in the US [7]. Brazil, US, and Argentina dominate soybean production around the world [8]. Soybean production has doubled during the last decade because of the increased income benefits to farmers and also because of the availability and diffusion of transgenic soybeans which are glyphosate resistant (first developed in 1998) [9, 10].

Soybean is affected by a plethora of diseases caused by bacteria, fungi and viruses as well as by pests such as insects and mites [11, 12]. The effect of diseases and pests on plants results in the reduction in soybean yield. For example, during 2014, the estimated loss due to diseases was 113 million bushels in 28 states in the US. Of this, losses caused by viruses were 11.6 million bushel [13, 14]. Forty-six viruses are known to infect soybeans [14], and among them eight are economically important viz., alfalfa mosaic virus (AMV), bean pod mottle virus (BPMV), peanut mottle virus (PeMoV), peanut stunt virus (PSV), soybean dwarf virus (SbDV), soybean mosaic virus (SMV), soybean vein necrosis virus (SVNV) and tobacco ringspot virus (TRSV) [13, 15].

## **2. Species** *soybean vein necrosis virus* **(tospoviridae: bunyavirales)***,* **history and dispersal in different continents of world**

In 2008, soybean vein necrosis orthotospovirus (SVNV) was first reported in Tennessee (US). To date, 22 US states have reported the virus presence [16–20], and the incidence of soybean vein necrosis disease in some states has been very high. For instance, in a 3-year survey conducted in the mid-west and mid-south US, it was reported that SVNV was present in 49/50 fields [21]. While this survey highlighted one of the most extreme cases of SVNV presence, in the United States the percent incidence ranged between 10 and 80 depending upon the plant stage and geographic areas. In 2012, the virus was also reported in Canada [22]. The genetic diversity of SVNV was studied from samples taken from different states and showed low variability. In 2013, a comparison of the nucleocapsid protein (NP) coding sequence of SVNV isolates collected from different states was done and it was found that it had 98–100% similarity [16]. At that time, it was proposed that the virus was new and might have been introduced into the US or recently might have been moved to soybeans from other plant hosts [16]. The spread of SVNV is not limited to North America, in fact in 2017, it was reported in Egypt (Middle East) [23] where its incidence was about 67%.

Interestingly, SVNV can spread through seed, an unusual feature for a tospovirus [24], and the US is one of the largest soybean exporters, making seed transmission a concern to importing countries. Until now it is speculated that due to transmission by seed and global soybean trade, seed may be a major source of virus transmission to the entire world [24]. This is because *Neohydatothrips variabilis* (Beach) and other secondary vectors, although dominant in Middle East and North America, are not abundant in other parts of the world such as Asia ([23–26]; **Figure 1**). Furthermore, it is unknown whether the virus is indigenous in importer countries because soybean has an Asian origin, so the disease may already be present in those countries but may have never been reported. Soybean vein necrosis disease symptoms are similar to many others caused by pathogens such as *Cercospora* and by other plant stresses, making its

**Figure 1.**

*World map showing thrips species distribution and soybean vein necrosis virus (SVNV) presence in different countries [23, 27–31].*

identification a challenge. A comprehensive survey of SVNV and its vectors in different countries is also missing. Until now *Frankliniella fusca* (Hinds), *N. variabilis* (Beach) and *Frankliniella tritici* (Fitch) have been found to be vectors of SVNV in the US [16, 32–34] but in Egypt *Megalurothrips sjostedii* (Trybom), *N. variabilis* (Beach), *F. occidentalis* (Pergande) and *Caliothrips phaseoli* (Hood) transmitted SVNV under experimental conditions [23].

## **2.1 Symptoms related to infection**

Infection by SVNV in soybean is characterized by necrosis of the veins as well as interveinal necrosis, followed by chlorosis of nearby leaf parenchyma [16, 35] (**Figure 2**). In 2013, a clear link between symptomology and virus association was described in soybean, which was confirmed later in various studies [16, 35], but some authors also found non-symptomatic SVNV positive soybeans plants [24], as well as an Asteraceae member, *Dendranthema grandiflorum,* which was virus positive using PCR [21, 35].

SVNV infection in soybean significantly reduces the oil content and may reduce the germination percentage, 100 seed weight (g), protein content percentage, and fiber content percentage [17]. An experiment was conducted to determine the seed transmission in discolored and damaged seeds, It showed that the virus was seed transmitted [24]. Another study conducted on mixed infection of SVNV and BPMV showed that both viruses can be present together as a mixed infection [25]. The seeds of BPMV infected soybean plants were also discolored. Interestingly BPMV is also seed transmitted [36]. It may be possible that both viruses used the same path to invade the seeds either through the developing embryo or any other route; however, research is needed in this context.

**Figure 2.**

*Symptoms related to infection. a) Uninfected plant leaf. b) Symptomatic plant inoculated with SVNV through mechanical inoculation performed with a syringe. c) SVNV symptomatic plants infected via thrips* N. variabilis *transmission.*

However, other studies conducted on the effect of SVNV on soybean yield determined that SVNV does not decrease the yield, but seed quality was affected [37]. Oil concentration was decreased by 0.1% with SVNV infection and linolenic acid, linoleic acid and stearic acid were increased [37]. This means that SVNV infection may result in lower marketability of soybean in high premium markets. In the oil market, a higher price is paid for seed which has lower linolenic acid and higher oleic acid. Bad quality seeds receive lower prices [17].

## **2.2 Alternative host range plants and their role as inoculum reservoirs**

Weeds provide a valuable natural means of virus survival when the soybean is not present. Alternative host plant studies of SVNV showed that the virus can infect chrysanthemum *D. grandiflorum* (Asteraceae), ivy-leaved morning glory *Ipomea hederacea* Jacq (Convolvulaceae), field pumpkin *Cucurbita pepo* (Cucurbitaceae), soybean *Glycine max* (Leguminosae), cowpea *Vigna unguiculata* (Leguminosae), mung bean *Vigna radiata* (Leguminosae), benthamiana *Nicotiana benthamiana* (Solanaceae), wild tobacco *Nicotiana tabacum* (Solanaceae)*,* tobacco *Nicotiana glutinosa* (Solanaceae) in the US [16]. However, in Egypt, ivy morning glory *Convolvulus arvensis* L. *Ipomea hederacea* Jacq (Convolvulaceae), soybean *G. max.* (Leguminosae) pulses *Lupinus sativum* (Leguminosae), mung beans *Vigna radiate* (Leguminosae), cheeseweed *Malva parviflora* L. *Portulaca oleraceae* (Portulaceae), benthamiana *N. benthamiana* (Solanaceae), tobacco *N. tabacum* (Solanaceae) are reported to serve as alternative hosts of SVNV [23]. Kudzu in the southern US States is a known overwintering host plant for the vector and virus [38].

#### **2.3 Seed transmission**

Seed transmission of viruses is a very complex phenomenon and is dependent upon the ability of a virus to penetrate the developing embryo as well as various factors including the type of host plant, time of infection of virus, amount of virus and mixed infection (compatibility of two viruses to propagate in the host plant cells at the same time) [39–43]. More than one hundred plant viruses are transmitted through seed [39, 44, 45]. Viruses often become difficult to control when they are transmitted through seed as well [39]. Virus transfer to the seed embryo can take place through different routes such as direct transfer, transfer through pollen, and indirect embryo invasion [39, 46]. Losses due to seed borne viruses increase when a stock of seed harboring virus is planted in a field [47].

There are contrary reports on the transmission of SVNV through seeds. One study conducted by Hajimurad [35] reported that like other orthotopsoviruses SVNV cannot be transmitted through seed but later in a study by Groves [24] found seed transmission and confirmed it through nested PCR and RNAseq. Hajimurad [35] did not find seed transmissibility and found only 1/1955 seeds were positive via ELISA. Hajimurad [35] considered that this observation was an anomaly and that SVNV is not seed transmitted. Another observation in the study by Hajimurad [35] was that all the seeds from the infected mother plants were non-symptomatic (not discolored or mottled, instead the seeds looked normal). However, Groves [24] used mottled and discolored seeds. Recently, a Zhou and Tzanetakis [25] study pointed that the mixed infection of SVNV and BPMV may lead to systemic infection of SVNV in the soybean seedlings. It may be that mixed infection of SVNV with BPMV results in the ability of SVNV to be seed transmitted. This is because it is hypothesized that SVNV uses the movement protein of the BPMV for systemic infection [25]. Although Zhou and Tzanetakis [48] also documented non-seed transmissibility of SVNV in 600 seedlings of field grown SVNV, most of the hybrid soybean seeds commercially available are not seed borne disease free. In SVNV, the seed transmission rate reported by Groves [24] is 6% which is considerable [24]. Until now, no virus belonging to Bunyavirales and Tosopoviridae has been regarded as a seed transmitted virus except SVNV*,* which gives SVNV a unique position among Tospoviridae [24, 49]. If the seed-transmission of SVNV is real, it would create a big challenge in the commercialization of soybean seeds for planting, especially in countries where SVNV is not present yet.

The avenue of seed transmission opens points for discussion. For example, if SVNV cannot be transmitted through seeds then how did the virus reach to the Middle East? It must be either human movement or thrips long distance migration. Further research is needed to confirm the seed transmissibility or the migration routes.

## **2.4 Disease diagnostics**

SVNV can be diagnosed with commercially available ELISA kits (for instance, Agdia, USA; & Life Technologies India). A Commercially available ELISA kits use synthesized antibodies. SVNV can also be diagnosed using PCR. Various authors have published PCR primers to amplify the different regions of the SVNV genome [16, 21, 50]. The variation in whole genome of SVNV can be measured through sequencing [21].

#### **2.5 Molecular characterization of SVNV**

SVNV is a spherical virus with a tri-segmented, negative-sense and ambisense, single-stranded RNA genome, containing 5 open reading frames [21, 51]. A schematic model of the SVNV virion based upon the literature [21, 24] is described in **Figure 3**. The diameter of the SVNV particles ranges between 80 and 100 nm [24]. The 3 genomic segments encode for putative proteins involved in virus replication, in plant defense evasion, virus movement in the plant, virus coating, and vector attachment [21]. The large segment (9010 nt) encodes for the putative RNAdependent RNA polymerase which is necessary for virus replication [21, 52]. The method of replication has been described in detail for tomato spotted wilt orthotospovirus (TSWV), the type species of this genus [52]. The middle segment (M) is 4955 nt long, ambisense and has two ORFs. ORF 1 encodes for a putative nonstructural movement protein (NSm). In TSWV infections, it is assumed that NSm makes tubular structures and is associated with plasmodesmata [53]. ORF 2 encodes

#### **Figure 3.**

*Model of soybean vein necrosis virus particles showing different RNA segments (small, medium and large) coated by N proteins. Glycoprotein (Gn, Gc) spikes decorating the lipid bilayer. Molecules of RNA dependent RNA polymerase (RdRP) are enclosed in the virus particles.*

for two putative glycoproteins, Gn and Gc, and their role in vector attachment has been well documented for TSWV [54]. Gn-Gc's role in the *F. occidentalis* and TSWV interaction showed that membrane mediated endocytosis takes place through interaction of Gc glycoproteins with a 50 kda thrips protein, while the Gn glycoprotein interacts with a 94 kda thrips protein [55]. As a result of this process virions move from the point of attachment in the midgut to the hemocoel and eventually to muscle cells, and from there to the salivary glands. The putative role of Gn-Gc glycoprotein in TSWV attachment was corroborated when antibodies raised against these proteins stopped virus acquisition and transmission [51]. Research on SVNV and *N. variabilis* interaction showed that the virus was present in the principal salivary gland, tubular salivary gland and the efferent duct of infected thrips [34].

The small segment (S) is ambisense, 2603 nt long, and contains two ORFs in opposite orientation [21]. ORF 1 encodes for the nonstructural silencing suppressor protein (NSs) [21]. This protein in TSWV binds dsRNA including miRNAs and siRNAs [52]. The role of NSs in SVNV and vector interaction still needs to be determined. ORF 2 encodes for the structural nucleocapsid protein (N) (31 kda) [21].

#### **2.6 SVNV and vector association**

Viruses belonging to Orthotospoviridae are persistent and propagative, which means that after entry into the vector insect, the virus multiplies in the insects and insects remain viruliferous for their entire life [54]. Studies conducted on the virus-vector relationship confirmed that *N. variabilis* (Beach.) is the primary vector of SVNV [16, 48]. The vector can acquire SVNV in the larval stages (L1 and L2) while only adults can transmit the virus [33], as for TSWV and other orthotopsoviruses. In addition, other thrips spp., *F. fusca*, *F. tritici, F. occidentalis, C. phaseoli* and *Megalurothrips sjostedti* can also transmit the virus [23]. In various experiments, transmission efficiency of vector thrips was evaluated. Keough,

Han [32] reported that *F. tritici*, and *F. fusca* transmission percentage ranges between 5% and 35% respectively. Han, Nalam [34] proved that SVNV-NP was present in the principal salivary gland, efferent duct, tubular salivary gland, and midgut region in the adult viruliferous thrips *F. tritici*, *F. fusca* and *N. variabilis* through immuno-labeling against SVNV NP. The virus was not observed in uninfected thrips species. Acquisition of orthotospoviruses in thrips and further transmission to the salivary gland and dispersal to uninfected plants is a complex process and involves the virus' ability to pass through the epithelial layer of the gut and then penetrate in the muscles and move through the tubular salivary gland to the efferent duct and the principal salivary glands [56, 57]. In *F. occidentalis* the contact between the salivary glands and the gut is closer in the first and second instar stage and later on when the insect grows to the pre-pupal and pupal stage the lack of contact is hypothesized to impede TSWV movement [57]. Although adult thrips can ingest the virus through feeding they cannot acquire the virus because the shift of virus to the salivary gland is not likely at the pupae and adult stages [57]. Also the tropism of virus replication shifts from the larval stages in the midgut epithelium to the salivary gland replication in the adult stages [57]. Moreover, the acquisition access time affects transmission of SVNV viz., transmission was higher after the 12 and 24 hrs acquisition access period (AAP) compared to 6 and 48 hrs AAP (Han, Nalam [34]).

Shazly [23] reported *F. occidentalis*, *C. phaseoli* and *M. sjostdi* can transmit SVNV with transmission efficiencies of 3.4, 6.7 and 3.3% respectively. However, major transmission of SVNV may be attributed mainly to *N. variabilis* as it was abundant in soybean crop in the US and Egypt compared to other species and due to higher transmission efficiency (70%) [23, 32, 33].

The host plant has a role in virus transmission. Shazly [23] stated that *N. variabilis* collected from cowpea can transfer virus 15% less efficiently than thrips collected from soybean. However, soybean thrips collected from mung bean had a transmission efficiency of 12.5%, while thrips collected from weeds such as *Melilotus indicus* and *Melochia corchiforia* can transfer virus with a transmission efficiency of 7.6 and 2.8% respectively [22].

There are complex theories regarding the thrips arrival, migration pattern, oviposition, hibernation and dispersion in the soybean fields (**Figures 1**–**4**) [21, 37]. According to Mueller, Higley [58] soybean thrips overwinter in southern states and annually migrate to northern US States (**Figure 4**). However, Anderson, Irizarry [17], and Zhou and Tzanetakis [48] postulated that due to the high number of thrips in soybean growing season in northern US states, soybean thrips may overwinter on perennial weeds and then during the early summer propagate on cover crops. Cover crops such as buckwheat and vegetables such as melon and winter pea can sustain SVNV and its vectors so they can act as reservoir to maintain inoculum from the overwintered insects and increase their number on the soybean crop [37, 59]. Irizarry, Elmore [59] proposed that alfalfa and other cover crops may act as the host of vectors before soybean planting in Wisconsin and Iowa. Zhou, Aboughanem-Sabanadzovic [38] suspected that Kudzu is a natural reservoir of SVNV and may be a natural shelter for the thrips during south to north movement every year because Kudzu is extensively present in the soybean growing region and interstate regions in the south.

Soybean is not thought to be the original host of SVNV because SVNV isolates collected in various locations on soybeans had more than 98% similarity [16]. However, comparison of the various isolates was done on the basis of the NP gene [16]. It would be interesting to look at the similarity of SVNV isolates in other genomic segments.

The SVNV transmission is complex because different vector species feed on different wild plants, weeds, cover crops and then eventually transfer the virus to the

#### **Figure 4.**

*Migration, dispersal and winter diapause of soybean theories, hypothesis and results. Here the yellow colored states are north eastern states. Light blue states = southern US states, purple = mid-west states, green = western states. This schematic diagram is based upon the Mueller, Higley [58] and Irizarry, Elmore [59] paper. Here the green leaf plant in southern states depict the weeds on which thrips overwinter in south and in the summer they migrate to the soybean crop in the north east and mid-west. However, according to Bloomingdale, Irizarry [60] the thrips do not migrate in the winter and they over winter on the weeds in the mid-west. However, in the northern states due to low temperature and snow the thrips cannot survive under the field conditions.*

target crop. Furthermore, the virus can also be transferred to other regions along with infected seeds (**Table 1**) [24].

Seasonally, many plants can support the thrips vector species and virus in various parts of the world until the principal crop is planted. A detailed study is needed in the spring and winter to examine the alternative host plants of vector and virus reservoirs. The detailed list of possible alternative host plants of the vector and their confirmation as the virus reservoir in different parts of the world is described in **Table 1**.







 *Alternative host plants of vector species in different parts of the world.*

**Table 1.**

## **2.7 Life cycle of** *N. variabilis* **(Beach)**

Soybean thrips lay eggs inside the leaf parenchymatous tissues near the leaf vein using a barbed ovipositor (**Figure 5**). A female lays about 70–90 eggs in her lifetime. Eggs hatch into first instar larvae having red eyes. These first instar larvae are transparent and feed on the leaf. The second instar larvae are pale yellow. The first instar duration is 3–4 days. Second and third instar duration is 2–3 days each. Fourth 4th instar duration is 2–4 days. Total adult male duration is 17–19 days and female duration is 20–23 days. Virus infection increased female survival [62]. Males are haploid. The mode of asexual reproduction is Arrehenotoky unlike *T. tabaci* L. where the mode of reproduction is deuterotoky.

#### **2.8 Management of SVNV and vector**

The importance of SVNV seems to be increasing. Several years ago, it was largely unknown, but recent studies have raised concerns about its severity. Management of seed and vector borne viruses requires complex knowledge of vector ecology, type of virus transmission (circulative, semi persistent, persistent), mode of virus introduction in the field (primary or secondary spread), the method of perception of the volatile compounds by insect sensillae, insect response to the plant released stressed volatile compounds, complex interaction between herbivores occupying same niche and threshold level of disease and vector as well [71]. Management considerations include:

1.The first step is always to start with clean seed. Planting damaged and discolored seeds may increase the chance of virus. Planting with mycorrhizae will

#### **Figure 5.**

*Life cycle of* N. variabilis. *The colored photographs were taken through the Olympus microscope 5RTV with colored CCD camera attached.*

increase plant vigor, canopy establishment, plant height, number and weight of nodules, number and weight of pods, total grain yield [72] and plant would be able to combat viruses and vector [72].


experimental conditions can pupate on leaves but in nature they pupate in the soil if it is available. We grew soybean thrips on plants and always found prepupae and pupal stage on leaves [62]. Some other thrips species do not move into soil and hence they can pupate on leaves, so we assume from our studies that fumigation of soil would not help reducing pest numbers however, this may help in greenhouse conditions to reduce *F. tritici* and *F. fusca* numbers.


## **3. Future research suggestions**


Gn and Gc glycoproteins may help to understand putative role of these viral proteins in thrips cells.



## **4. Conclusion**

Soybean vein necrosis virus is an important seed and vector transmitted virus present in middle East, US and Canada. This virus can decrease the oil content percentage. SVNV can be transmitted through different species of thrips. Among them *N. variabilis* is an important vector. SVNV has also been reported in various species of weeds where it can over winter. In the US, Kudzu is an important interstate virus reservoir for migrating thrips. Although various species of thrips can transmit SVNV, the rate of transmission of *N. variabilis* is considerably higher. SVNV is a negative sense single stranded RNA virus that can replicate in thrips and plants. Management of SVNV must be strategized as the vector and virus colonization on double beans can lower plant yield. Hence monitoring of thrips population using yellow sticky cards, and application of new chemistry insecticides should be done on late planted soybeans to reduce the pest pressure on double cropped soybeans. Future research is needed to understand the mechanism of propagation of SVNV in plant seeds, development of resistant varieties, exploring the role of Gn rich transgenic soybeans, and of gene silencing, a method that could be used to control SVNV.

#### **Acknowledgements**

The authors would like to acknowledge the Fulbright grant for PhD studies of the first author. We also wish to acknowledge the Pennsylvania Soybean Board (PSB) for providing funds for graduate student research (PSB #199751).

*Legumes Research - Volume 1*

## **Conflict of interest**

The authors declare that there are no conflicts of interest.

## **Author details**

Asifa Hameed1 \*, Cristina Rosa<sup>2</sup> and Edwin G. Rajotte1

1 Department of Entomology, The Pennsylvania State University, University Park, USA

2 Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, USA

\*Address all correspondence to: asifa\_hameed\_sheikh@yahoo.com

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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## **Chapter 19**
