Bees are important plant pollinators in agricultural and natural ecosystems. High average annual losses of honey bee (Apis mellifera) colonies in some parts of the world, and regional population declines of some mining bee species (Andrena spp.), are attributed to multiple factors including habitat loss, lack of quality forage, insecticide exposure, and pathogens, including viruses. While research has primarily focused on viruses in honey bees, many of these viruses have a broad host range. It is therefore important to apply a community level approach in studying the epidemiology of bee viruses. We utilized high-throughput sequencing to evaluate viral diversity and viral sharing in sympatric, co-foraging bees in the context of habitat type. Variants of four common viruses (i.e., black queen cell virus, deformed wing virus, Lake Sinai virus 2, and Lake Sinai virus NE) were identified in honey bee and mining bee samples, and the high degree of nucleotide identity in the virus consensus sequences obtained from both taxa indicates virus sharing. We discovered a unique bipartite + ssRNA Tombo-like virus, Andrena-associated bee virus-1 (AnBV-1). AnBV-1 infects mining bees, honey bees, and primary honey bee pupal cells maintained in culture. AnBV-1 prevalence and abundance was greater in mining bees than in honey bees. Statistical modeling that examined the roles of ecological factors, including floral diversity and abundance, indicated that AnBV-1 infection prevalence in honey bees was greater in habitats with low floral diversity and abundance, and that interspecific virus transmission is strongly modulated by the floral community in the habitat. These results suggest that land management strategies that aim to enhance floral diversity and abundance may reduce AnBV-1 spread between co-foraging bees.
Plant pathogens, including viruses, negatively impact global crop production. Plants have evolved complex immune responses to pathogens. These responses are often controlled by nucleotide-binding leucine-rich repeat proteins (NLRs), which recognize intracellular, pathogen-derived proteins. Genetic resistance to plant viruses is often phenotypically characterized by programmed cell death at or near the infection site; a reaction termed the hypersensitive response. Although visualization of the hypersensitive response is often used as a hallmark of resistance, the molecular mechanisms leading to the hypersensitive response and associated cell death vary. Plants with extreme resistance to viruses rarely exhibit symptoms and have little to no detectable virus replication or spread beyond the infection site. Both extreme resistance and the hypersensitive response can be activated by the same NLR genes. In many cases, genes that normally provide an extreme resistance phenotype can be stimulated to cause a hypersensitive response by experimentally increasing cellular levels of pathogen-derived elicitor protein(s). The molecular mechanisms of extreme resistance and its relationship to the hypersensitive response are largely uncharacterized. Studies on potato and soybean cultivars that are resistant to strains of Potato virus Y (PVY), Potato virus X (PVX), and Soybean mosaic virus (SMV) indicate that abscisic acid (ABA)-mediated signaling and NLR nuclear translocation are important for the extreme resistance response. Recent research also indicates that some of the same proteins are involved in both extreme resistance and the hypersensitive response. Herein, we review and synthesize published studies on extreme resistance in potato and soybean, and describe studies in additional species, including model plant species, to highlight future research avenues that may bridge the gaps in our knowledge of plant antiviral defense mechanisms.
Potato virus Y (PVY) infection is one of the greatest challenges to seed potato production in the United States. To determine how cultivar and seed type affect the development of systemic PVY infection, Russet Burbank and Russet Norkotah Colorado 3 cultivars were grown from two types of pre-nuclear seed (i.e., plantlets and minitubers) and Generation 3 (G3) tubers and challenged with PVY strain Wilga (PVY N-Wi ). Systemic PVY infection was measured by assaying spread of virus from the inoculation site to upper non-inoculated leaves. The Burbank cultivar had a lower incidence of systemic PVY infection compared to the incidence of systemic PVY that developed in the Colorado 3 cultivar. Furthermore, Burbank plants grown from G3 tubers had a lower incidence of systemic PVY infection, as compared to Burbank plants grown from plantlets. Together our results indicate that both cultivar and seed type affect the development of systemic PVY N-Wi infections post-inoculation. ResumenLa infección por virus Y (PVY) es uno de los mayores retos en la producción de semilla de papa en los Estados Unidos. Para determinar cómo afecta la variedad y el tipo de semilla al desarrollo de la infección sistémica de PVY, se cultivaron las variedades Russet Burbank y Russet Norkotah Colorado 3 de dos tipos de semilla pre-nuclear (p. e., plántulas y minitubérculos) y de tubérculos de la Generación 3 (G3), y se inocularon con PVY variante Wilga (PVYN-Wi). La infección sistémica de PVY se midió mediante la detección de la dispersión del virus desde el sitio de inoculación hacia las hojas superiores no inoculadas. La variedad Burbank tuvo la incidencia más baja de infección sistémica de PVYen comparación con la incidencia de PVY sistémico que se desarrolló en la variedad Colorado 3. Aún más, las plantas de Burbank originadas de los tubérculos de G3 tuvieron la incidencia más baja de infección sistémica de PVY, en comparación con las plantas de Burbank originadas de plántulas. Juntos, nuestros resultados indican que tanto la variedad como el tipo de semilla afectan el desarrollo de infecciones sistémicas de PVYN-Wi después de la inoculación.
Potatoes are the world’s most produced non-grain crops and an important food source for billions of people. Potatoes are susceptible to numerous pathogens that reduce yield, including Potato virus Y (PVY). Genetic resistance to PVY is a sustainable way to limit yield and quality losses due to PVY infection. Potato cultivars vary in their susceptibility to PVY and include susceptible varieties such as Russet Burbank, and resistant varieties such as Payette Russet. Although the loci and genes associated with PVY-resistance have been identified, the genes and mechanisms involved in limiting PVY during the development of systemic infections have yet to be fully elucidated. To increase our understanding of PVY infection, potato antiviral responses, and resistance, we utilized RNA sequencing to characterize the transcriptomes of two potato cultivars. Since transcriptional responses associated with the extreme resistance response occur soon after PVY contact, we analyzed the transcriptome and small RNA profile of both the PVY-resistant Payette Russet cultivar and PVY-susceptible Russet Burbank cultivar 24 h post-inoculation. While hundreds of genes, including terpene synthase and protein kinase encoding genes, exhibited increased expression, the majority, including numerous genes involved in plant pathogen interactions, were downregulated. To gain greater understanding of the transcriptional changes that occur during the development of systemic PVY-infection, we analyzed Russet Burbank leaf samples one week and four weeks post-inoculation and identified similarities and differences, including higher expression of genes involved in chloroplast function, photosynthesis, and secondary metabolite production, and lower expression of defense response genes at those time points. Small RNA sequencing identified different populations of 21- and 24-nucleotide RNAs and revealed that the miRNA profiles in PVY-infected Russet Burbank plants were similar to those observed in other PVY-tolerant cultivars and that during systemic infection ~32% of the NLR-type disease resistance genes were targeted by 21-nt small RNAs. Analysis of alternative splicing in PVY-infected potato plants identified splice variants of several hundred genes, including isoforms that were more dominant in PVY-infected plants. The description of the PVYN-Wi-associated transcriptome and small RNA profiles of two potato cultivars described herein adds to the body of knowledge regarding differential outcomes of infection for specific PVY strain and host cultivar pairs, which will help further understanding of the mechanisms governing genetic resistance and/or virus-limiting responses in potato plants.
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