Viruses Infecting Trees and Herbs That Produce Edible Fleshy Fruits with a Prominent Value in the Global Market: An Evolutionary Perspective

Trees and herbs that produce fruits represent the most valuable agricultural food commodities in the world. However, the yield of these crops is not fully achieved due to biotic factors such as bacteria, fungi, and viruses. Viruses are capable of causing alterations in plant growth and development, thereby impacting the yield of their hosts significantly. In this work, we first compiled the world′s most comprehensive list of known edible fruits that fits our definition. Then, plant viruses infecting those trees and herbs that produce fruits with commercial importance in the global market were identified. The identified plant viruses belong to 30 families, most of them containing single-stranded RNA genomes. Importantly, we show the overall picture of the host range for some virus families following an evolutionary approach. Further, the current knowledge about plant-virus interactions, focusing on the main disorders they cause, as well as yield losses, is summarized. Additionally, since accurate diagnosis methods are of pivotal importance for viral diseases control, the current and emerging technologies for the detection of these plant pathogens are described. Finally, the most promising strategies employed to control viral diseases in the field are presented, focusing on solutions that are long-lasting.

Differential Synergistic Interactions Among Four Different Wheat-Infecting Viruses

Field-grown wheat (Triticum aestivum L.) plants can be co-infected by multiple viruses, including wheat streak mosaic virus (WSMV), Triticum mosaic virus (TriMV), brome mosaic virus (BMV), and barley stripe mosaic virus (BSMV). These viruses belong to four different genera in three different families and are, hence, genetically divergent. However, the impact of potential co-infections with two, three, or all four of them on the viruses themselves, as well as the wheat host, has yet to be examined. This study examined bi-, tri-, and quadripartite interactions among these viruses in wheat for disease development and accumulation of viral genomic RNAs, in comparison with single virus infections. Co-infection of wheat by BMV and BSMV resulted in BMV-like symptoms with a drastic reduction in BSMV genomic RNA copies and coat protein accumulation, suggesting an antagonism-like effect exerted by BMV toward BSMV. However, co-infection of either BMV or BSMV with WSMV or TriMV led to more severe disease than singly infected wheat, but with a decrease or no significant change in titers of interacting viruses in the presence of BMV or BSMV, respectively. These results were in stark contrast with exacerbated disease phenotype accompanied with enhanced virus titers caused by WSMV and TriMV co-infection. Co-infection of wheat by WSMV, TriMV, and BMV or BSMV resulted in enhanced synergistic disease accompanied by increased accumulation of TriMV and BMV but not WSMV or BSMV. Quadripartite interactions in co-infected wheat by all four viruses resulted in very severe disease synergism, leading to the death of the most infected plants, but paradoxically, a drastic reduction in BSMV titer. Our results indicate that interactions among different viruses infecting the same plant host are more complex than previously thought, do not always entail increases in virus titers, and likely involve multiple mechanisms. These findings lay the foundation for additional mechanistic dissections of synergistic interactions among unrelated plant viruses.

Barley stripe mosaic virus γb protein targets thioredoxin h-type 1 to dampen SA-mediated antiviral defenses

Salicylic acid (SA) acts as a signaling molecule to perceive and defend against pathogen infections. Accordingly, pathogens evolve versatile strategies to disrupt the SA-mediated signal transduction. However, it is necessary to further characterize how plant viruses manipulate the SA-dependent defense responses. Here, we show that Barley stripe mosaic virus (BSMV) infection activates SA-mediated defense signaling pathway and upregulates the expression of Nicotiana benthamiana thioredoxin h-type 1 (NbTRXh1). The γb protein interacts directly with NbTRXh1 in vivo and in vitro. Overexpression of NbTRXh1, but not a reductase-defective mutant, impedes BSMV infection, whereas low NbTRXh1 expression level results in increased viral accumulation. Similar with its orthologues in Arabidopsis, NbTRXh1 also plays an essential role in SA signaling transduction in N. benthamiana. To counteract NbTRXh1-mediated defenses, the BSMV ?b protein targets NbTRXh1 to dampen its reductase activity and thereby impairing downstream SA defense genes expression to optimize viral cell-to-cell movement. We also found that NbTRXh1-mediated resistance defends against Lychnis ringspot virus, Beet black scorch virus, and Beet necrotic yellow vein virus. Taken together, our results reveal a novel role for the multifunctional γb protein in counteracting plant defense responses, and broadens the broad-spectrum antibiotic role of SA signaling pathway.

Comparative plant transcriptome profiling of Arabidopsis and Camelina infested with Myzus persicae aphids acquiring circulative and non-circulative viruses reveals virus- and plant-specific alterations relevant to aphid feeding behavior and transmission

Background: Evidence accumulates that plant viruses alter host-plant traits in ways that modify their insect vectors' behavior. These alterations often enhance virus transmission, which has led to the hypothesis that these effects are manipulations caused by viral adaptation. However, the genetic basis of these indirect, plant-mediated effects on vectors and their dependence on the plant host and the mode of virus transmission is hardly known. Results: Transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with turnip yellows virus (TuYV) or cauliflower mosaic virus (CaMV) and infested with the common aphid vector Myzus persicae revealed strong virus- and host-specific differences in the gene expression patterns. CaMV infection caused more severe effects on the phenotype of both plant hosts than did TuYV infection, and the severity of symptoms correlated strongly with the proportion of differentially expressed genes, especially photosynthesis genes. Accordingly, CaMV infection modified aphid behavior and fecundity stronger than did infection with TuYV. Conclusions: Overall, infection with CaMV — relying on the non-circulative transmission mode — tends to have effects on metabolic pathways with strong potential implications for insect-vector / plant-host interactions (e.g. photosynthesis, jasmonic acid, ethylene and glucosinolate biosynthetic processes), while TuYV — using the circulative transmission mode — alters these pathways only weakly. These virus-induced deregulations of genes that are related to plant physiology and defense responses might impact aphid probing and feeding behavior on both infected host plants, with potentially distinct effects on virus transmission. Keywords: Caulimovirus, polerovirus, aphid vector, transmission, feeding behavior, insect-plant interactions, transcriptome profiling, RNA-seq.

Role of Sw5 gene cluster in the fight against plant viruses

The Sw5 gene cluster furnishes robust resistance to Tomato spotted wilt virus in tomato, which has led to its widespread applicability in agriculture. Among the five orthologs, Sw5b functions as a resistance gene against a broad-spectrum Tospovirus and is linked with Tospovirus resistance. However, its paralog, Sw5a, has been recently implicated in providing resistance against Tomato leaf curl New Delhi virus , broadening the relevance of the Sw5 gene cluster in promoting defense against plant viruses. We propose that plants have established modifications within the homologs of R genes that permit identification of different effector proteins and provide broad and robust resistance against different pathogens through activation of hypersensitive response and cell death.

Field application of nanoliposomes delivered quercetin by inhibiting specific hsp70 gene expression against plant virus disease

Background The annual economic loss caused by plant viruses exceeds 10 billion dollars due to the lack of ideal control measures. Quercetin is a flavonol compound that exerts a control effect on plant virus diseases, but its poor solubility and stability limit the control efficiency. Fortunately, the development of nanopesticides has led to new ideas. Results In this study, 117 nm quercetin nanoliposomes with excellent stability were prepared from biomaterials, and few surfactants and stabilizers were added to optimize the formula. Nbhsp70er-1 and Nbhsp70c-A were found to be the target genes of quercetin, through abiotic and biotic stress, and the nanoliposomes improved the inhibitory effect at the gene and protein levels by 33.6 and 42%, respectively. Finally, the results of field experiment showed that the control efficiency was 38% higher than that of the conventional quercetin formulation and higher than those of other antiviral agents. Conclusion This research innovatively reports the combination of biological antiviral agents and nanotechnology to control plant virus diseases, and it significantly improved the control efficiency and reduced the use of traditional chemical pesticides. Graphical Abstract

N6-Methyladenosine Regulatory Machinery is Involved In Viral Infection of Plum Pox Virus And Potato Virus Y In Nicotiana Benthamiana

Abstract N6-methyladenosine (m6A) is a post-transcriptional modification of biological mRNA and non-coding RNAs, which by regulating the mRNA stability and translation. It has been demonstrated that m6A methylation has a regulatory effect on human RNA virus replication. In this project, Plum pox virus (PPV) and Potato Y virus (PVY) were used to examine the m6A modification in Nicotiana benthamiana during natural infection. The results showed that the global level of m6A in both PVY and PPV infected plants were significantly decreased than non-infected plants. Particularly, the PPV and PVY infection could alter the m6A level of the host endogenous gene. This is suggesting that plant viruses may disrupt the balance of the m6A in plant. Meanwhile, we found that viral genome RNA can be targeted by m6A methylation. Two m6A-enrich regions in PPV genome RNA and four in PVY genome RNA were detected, which are located in the coding region of viruses. Based on the ALKB and METTL sequences in the transcriptome sequencing data of the virus-infected plant, we cloned 2 NbALKB genes and 2 NbMETTL genes in N. benthamiana . According to results of transient expression and VIGS assay, NbALKB gene appears slightly contributing PPV and PVY infection. NbMETTL gene showed certain inhibition effect in PPV infection, but not PVY. Therefore, our data suggested that m6A methylation in plant might be an anti-viral strategy in some plant viruses.

Evaluation of the Chilli veinal mottle virus CP gene expressing transgenic Nicotiana benthamiana plants for disease resistance against the virus

Vegetables are an important source of income and high-value crops for small farmers. Chilli (Capsicum spp.) is one of the most economically important vegetables of Pakistan and it is grown throughout the country. It is a rich source of nutrition especially vitamins A, B, C and E along with minerals as folic acid, manganese (Mn), potassium (K) and molybdenum (Mo). Chilli possesses seven times more amount of vitamin C than an orange. Vitamin A, C and beta-carotenoids are strong antioxidants to scavenge the free radicals. Chilli production is restricted due to various biotic factors. Among these viruses, Chilli veinal mottle virus (ChiVMV) is one of the most destructive and menacing agents that inflicts heavy and colossal losses that accounted for 50% yield loss both in quality and quantity. Pathogen-Derived Resistance (PDR) approach is considered one of the effective approaches to manage plant viruses. In this study, ChiVMV was characterized on a molecular level, the coat protein (CP) gene of the virus was stably transformed into Nicotiana benthamiana plants using Agrobacterium tumefaciens. The transgenic plants were challenged with the virus to evaluate the level of resistance of plants against the virus. It was observed that the plants expressing CP gene have partial resistance against the virus in terms of symptoms’ development and virus accumulation. Translation of this technique into elite chilli varieties will be resulted to mitigate the ChiVMV in the crop as well as an economic benefit to the farmers.

Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission

Many plant viruses are transmitted by insect vectors. Transmission can be described as persistent or non-persistent depending on rates of acquisition, retention, and inoculation of virus. Much experimental evidence has accumulated indicating vectors can prefer to settle and/or feed on infected versus noninfected host plants. For persistent transmission, vector preference can also be conditional, depending on the vector’s own infection status. Since viruses can alter host plant quality as a resource for feeding, infection potentially also affects vector population dynamics. Here we use mathematical modelling to develop a theoretical framework addressing the effects of vector preferences for landing, settling and feeding–as well as potential effects of infection on vector population density–on plant virus epidemics. We explore the consequences of preferences that depend on the host (infected or healthy) and vector (viruliferous or nonviruliferous) phenotypes, and how this is affected by the form of transmission, persistent or non-persistent. We show how different components of vector preference have characteristic effects on both the basic reproduction number and the final incidence of disease. We also show how vector preference can induce bistability, in which the virus is able to persist even when it cannot invade from very low densities. Feedbacks between plant infection status, vector population dynamics and virus transmission potentially lead to very complex dynamics, including sustained oscillations. Our work is supported by an interactive interface https://plantdiseasevectorpreference.herokuapp.com/. Our model reiterates the importance of coupling virus infection to vector behaviour, life history and population dynamics to fully understand plant virus epidemics.