Diverse Begomoviruses Evolutionarily Hijack Plant Terpenoid-Based Defense to Promote Whitefly Performance
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Arthropod-borne pathogens and parasites are major threats to human health and global agriculture. They may directly or indirectly manipulate behaviors of arthropod vector for rapid transmission between hosts. The largest genus of plant viruses, Begomovirus, is transmitted exclusively by whitefly (Bemisia tabaci), a complex of at least 34 morphologically indistinguishable species. We have previously shown that plants infected with the tomato yellowleaf curl China virus (TYLCCNV) and its associated betasatellite (TYLCCNB) attract their whitefly vectors by subverting plant MYC2-regulated terpenoid biosynthesis, therefore forming an indirect mutualism between virus and vector via plant. However, the evolutionary mechanism of interactions between begomoviruses and their whitefly vectors is still poorly understood. Here we present evidence to suggest that indirect mutualism may happen over a millennium ago and at present extensively prevails. Detailed bioinformatics and functional analysis identified the serine-33 as an evolutionary conserved phosphorylation site in 105 of 119 Betasatellite species-encoded βC1 proteins, which are responsible for suppressing plant terpenoid-based defense by interfering with MYC2 dimerization and are essential to promote whitefly performance. The substitution of serine-33 of βC1 proteins with either aspartate (phosphorylation mimic mutants) or cysteine, the amino acid in the non-functional sβC1 encoded by Siegesbeckia yellow vein betasatellite SiYVB) impaired the ability of βC1 functions on suppression of MYC2 dimerization, whitefly attraction and fitness. Moreover the gain of function mutation of cysteine-31 to serine in sβC1 protein of SiYVB restored these functions of βC1 protein. Thus, the dynamic phosphorylation of serine-33 in βC1 proteins helps the virus to evade host defense against insect vectors with an evolutionarily conserved manner. Our data provide a mechanistic explanation of how arboviruses evolutionarily modulate host defenses for rapid transmission.Keywords:
Whitefly
Mutualism
BACKGROUND The whitefly Bemisia tabaci (Gennadius) is considered one of the main pests for agriculture. One important problem with the whitefly is its notorious status as a vector for plant viruses, primarily begomoviruses. We have previously identified a defensin-like antimicrobial peptide, Btdef, from the whitefly B. tabaci MEAM1. However, the function of Btdef in the immune system of the insect vector and begomovirus transmission has yet to be explored. RESULTS To explore the role of Btdef during begomovirus transmission, we firstly investigated the transcriptional response of Btdef following acquisition of Tomato yellow leaf curl China virus (TYLCCNV). The expression of Btdef was up-regulated in the viruliferous whiteflies. After RNA silencing of the Btdef gene in adult whiteflies fed with dsRNA, they were allowed to feed on TYLCCNV-infected plants and then quantified for TYLCCNV DNA titre. Unexpectedly, silencing the Btdef gene reduced both the abundance and expressions of TYLCCNV genes in the whiteflies. In the meantime, the density of the endosymbiont Rickettsia was significantly reduced in dsBtdef-fed whiteflies. CONCLUSION Our data provide evidence that Btdef is involved in begomovirus infection, possibly through symbiont-mediated alteration of begomovirus–whitefly interactions. These findings indicate that Btdef may be targeted for the development of new technology for the control of whitefly-transmitted begomoviruses. © 2016 Society of Chemical Industry
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Abstract Background Many plant viruses are vector-borne and depend on arthropods for transmission between host plants. Begomoviruses, the largest, most damaging and emerging group of plant viruses, infect hundreds of plant species, and new virus species of the group are discovered each year. Begomoviruses are transmitted by members of the whitefly Bemisia tabaci species complex in a persistent-circulative manner. Tomato yellow leaf curl virus (TYLCV) is one of the most devastating begomoviruses worldwide and causes major losses in tomato crops, as well as in many agriculturally important plant species. Different B. tabaci populations vary in their virus transmission abilities; however, the causes for these variations are attributed among others to genetic differences among vector populations, as well as to differences in the bacterial symbionts housed within B. tabaci. Results Here, we performed discovery proteomic analyses in 9 whitefly populations from both Middle East Asia Minor I (MEAM1, formerly known as B biotype) and Mediterranean (MED, formerly known as Q biotype) species. We analysed our proteomic results on the basis of the different TYLCV transmission abilities of the various populations included in the study. The results provide the first comprehensive list of candidate insect and bacterial symbiont (mainly Rickettsia) proteins associated with virus transmission. Conclusions Our data demonstrate that the proteomic signatures of better vector populations differ considerably when compared with less efficient vector populations in the 2 whitefly species tested in this study. While MEAM1 efficient vector populations have a more lenient immune system, the Q efficient vector populations have higher abundance of proteins possibly implicated in virus passage through cells. Both species show a strong link of the facultative symbiont Rickettsia to virus transmission.
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Whitefly vector insects can spread the Pepper yellow leaf curl Indonesia virus (PYLCIV) that causes Begomovirus disease. One whitefly can transmit the virus, which belongs to the Begomovirus genus. It is suspected that the more whitefly, the higher the incidence and severity of Begomovirus disease. The increased severity of Begomovirus disease can affect chili yields. This study aimed to assess the relationship between the whitefly population level, the Begomovirus disease's intensity, and the production of chili peppers. The research method used was a survey of the farmers' chili plantations. Observations of the whitefly population and disease intensity were carried out on a scheduled basis. The results showed that the whitefly population affected the incidence and severity of the disease Begomovirus. Each addition of one whitefly/leaf will increase the incidence of disease by 25.981%, the severity by 15.269%, and reduce the yield of chili plants by 40.044 kg/ha. Meanwhile, every 1% increase in the severity of Begomovirus disease will reduce the production of chili plants by 2.867 kg/ha.
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Over the last 20 years, begomoviruses have emerged as devastating pathogens, limiting the production of different crops worldwide. Weather conditions increase vector populations, with negative effects on crop production. In this work we evaluate the relationship between the incidence of begomovirus and weather before and during the crop cycle. Soybean and bean fields from north-western (NW) Argentina were monitored between 2001 and 2018 and classified as moderate (≤50%) or severe (>50%) according to the begomovirus incidence. Bean golden mosaic virus (BGMV) and soybean blistering mosaic virus (SbBMV) were the predominant begomovirus in bean and soybean crops, respectively. Nearly 200 bio-meteorological variables were constructed by summarizing climatic variables in 10-day periods from July to November of each crop year. The studied variables included temperature, precipitation, relative humidity, wind (speed and direction), pressure, cloudiness, and visibility. For bean, high maximum winter temperatures, low spring humidity, and precipitation 10 days before planting correlated with severe incidence. In soybeans, high temperatures in late winter and in the pre-sowing period, and low spring precipitations were found to be good predictors of high incidence of begomovirus. The results suggest that temperature and pre-sowing precipitations can be used to predict the incidence status [predictive accuracy: 80% (bean) and 75% (soybean)]. Thus, these variables can be incorporated in early warning systems for crop management decision-making to reduce the virus impact on bean and soybean crops.
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The indirect interactions between insect vectors, such as whiteflies, and the viruses they transmit, such as begomoviruses, via host plants may produce a range of outcome depending on the species/strain of each of the three organisms involved, and the mechanisms underlying the variations are not well understood. Here, we observed the performance of whiteflies on three types of tomato, which vary in level of jasmonic acid (JA)-related resistance and were either uninfected or infected by a begomovirus, to investigate the role of JA-related resistance in mediating whitefly-begomovirus interactions. Compared to the performance of whiteflies on plants of the wild type, the performance was elevated on plants deficient in JA-related resistance but reduced on plants with a high level of JA-related resistance. Further, on plants with a high level of JA-related resistance, the whitefly performed better on virus-infected than on uninfected plants; however, on tomato plants deficient in JA-related resistance, whitefly performance was less affected by the virus-infection of plants. Additionally, the expression of the JA-regulated defense gene PI-II in tomato plants was repressed by virus infection. These findings suggest that JA-related resistance plays an important role in the tripartite interactions between whitefly, begomovirus and tomato plant.
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Tomato yellow leaf curl virus (TYLCV) (Begomovirus, Geminiviridae) is the type member and representative of the complex of viruses associated with the tomato yellow leaf curl disease (TYLCD) with ssDNA genome, a plant-infecting group of viruses that have single or double genomic components enveloped by an icosahedral coat protein. These viruses infect tomatoes and other vegetable and ornamental crops and cause severe losses estimated by billions of dollars each year. Begomoviruses are exclusively transmitted by the whitefly Bemisia tabaci in a persistent circulative manner. First epidemics of TYLCV were reported in Israel in the early 1960s and later on the causative agent was identified as TYLCV. Epidemics were often associated with the presence of whiteflies. Since then, extensive research in many laboratories in the world was conducted to better understand the interactions between TYLCV, the tomato plant and its only vector B. tabaci. These studies resulted in hundreds of research papers and reviews, a...
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Leaf curl
Geminiviridae
Ornamental plant
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Myrmecophyte
Defence mechanisms
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