Vector acquisition and co-inoculation of two plant viruses influences transmission, infection, and replication in new hosts

McLaughlin, Autumn; Hanley‐Bowdoin, Linda; Kennedy, George G.; Jacobson, Alana L.

doi:10.1038/s41598-022-24880-5

Cited by 9 publications

(10 citation statements)

References 91 publications

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“…Recently, McLaughlin et al (2022) reported experiments on transmission, infection, and replication of tomato yellow leaf curl virus (TYLC) and tomato mottle virus (ToMoV) in tomato: data on acquisition and co-inoculation by B. tabaci were found to be fundamental in disentangling the vector-virus-host interaction and the spread of single and co-infections.…”

Section: Vector Transmission and Co-infecting Plant Virusesmentioning

confidence: 99%

Emerging Themes and Approaches in Plant Virus Epidemiology

2023

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Plant diseases caused by viruses share many common features with those caused by other pathogen taxa in terms of the host-pathogen interaction, but there are also distinctive features in epidemiology, most apparent where transmission is by vectors. Consequently, the host-virus-vector-environment interaction presents a continuing challenge in attempts to understand and predict the course of plant virus epidemics. Theoretical concepts, based on the underlying biology, can be expressed in mathematical models, and tested through quantitative assessments of epidemics in the field; this remains a goal in understanding why plant virus epidemics occur and how they can be controlled. To this end, this review identifies recent emerging themes and approaches to fill in knowledge gaps in plant virus epidemiology. We review quantitative work on impact of climatic fluctuations and change on plants, virus and vectors under different scenarios where impacts on the individual components of the plant-virus-vector interaction may vary disproportionately; the continuing sometimes discordant debate on host resistance and tolerance as plant defense mechanisms, including aspects of farmer behavior and attitudes to disease management that may affect deployment in crops; disentangling host-virus-vector-environment interactions as these contribute to temporal and spatial disease progress in field populations, computational techniques for estimating epidemiological parameters from field observations, and the use of optimal control analysis to assess disease control options. We end by proposing new challenges and questions in plant virus epidemiology.

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Section: Vector Transmission and Co-infecting Plant Virusesmentioning

confidence: 99%

Emerging Themes and Approaches in Plant Virus Epidemiology

2023

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“…For example, pepper huasteco yellow vein virus (PHYVV) and pepper golden mosaic virus (PGMV) can be co-transmitted by Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) to pepper plants without competition [ 67 ]. Similarly, no competition was identified between two strains of tomato yellow leaf curl virus (TYLCV) in B. tabaci [ 68 ], but TYLCV and tomato mottle virus (ToMoV) competed when transmitted by B. tabaci [ 25 ]. Specific regions within the begomovirus coat protein are involved in the interaction with the gut and salivary gland receptors in the whitefly vectors [ 69 , 70 , 71 ].…”

Section: Are Closely Related Pathogens More Likely To Compete During ...mentioning

confidence: 99%

“…Similar problems exist to evaluate if the pathogens were effectively transmitted: a reduction in the transmission efficiency of a pathogen could result from competition between pathogens in the vector or during the infection of the recipient plant. Artificial diets instead of recipient plants can be used to overcome some of these issues [ 25 ]; however, this approach has caveats as described above. Further, the use of artificial diets might affect the detachment of the pathogen from vector receptors.…”

Section: Co-transmission: a Complex System Without A Simple Solutionmentioning

confidence: 99%

“…Alternatively, it could result in increased transmission if one pathogen facilitates the transmission of the other by acting as a helper virus [ 23 ]. Excellent studies have previously reported or reviewed several examples of co-transmission of plant pathogens, such as [ 24 ] or [ 25 ]. Therefore, the present review is not a comprehensive review of all the co-transmission studies published, just of a few which allow us to showcase new findings and identify challenges encountered in the study of co-transmission as well as future perspectives.…”

Section: Introductionmentioning

confidence: 99%

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A New Perspective on the Co-Transmission of Plant Pathogens by Hemipterans

et al. 2023

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Co-infection of plants by pathogens is common in nature, and the interaction of the pathogens can affect the infection outcome. There are diverse ways in which viruses and bacteria are transmitted from infected to healthy plants, but insects are common vectors. The present review aims to highlight key findings of studies evaluating the co-transmission of plant pathogens by insects and identify challenges encountered in these studies. In this review, we evaluated whether similar pathogens might compete during co-transmission; whether the changes in the pathogen titer in the host, in particular associated with the co-infection, could influence its transmission; and finally, we discussed the pros and cons of the different approaches used to study co-transmission. At the end of the review, we highlighted areas of study that need to be addressed. This review shows that despite the recent development of techniques and methods to study the interactions between pathogens and their insect vectors, there are still gaps in the knowledge of pathogen transmission. Additional laboratory and field studies using different pathosystems will help elucidate the role of host co-infection and pathogen co-transmission in the ecology and evolution of infectious diseases.

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“…Plant traits modified by infection or multi-infection can have consequences on virus transmission because they can change the nutritional quality of the plant or modify visual traits and production of volatiles that play important roles in vector-plant interactions. These alterations of the multi-infected plants can therefore influence vector behavior and subsequently virus transmission (Mauck et al, 2012; Mauck et al, 2016; McLaughlin et al, 2022; Moreno & López-Moya, 2020) . Studies on mixed viral infections with regard to vector interaction and transmission are scarce.…”

Section: Introductionmentioning

confidence: 99%

Interplay between a polerovirus and a closterovirus decreases aphid transmission of the polerovirus

Khechmar,

Chesnais,

Villeroy

et al. 2024

Preprint

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Multi-infection of plant by viruses is very common and can change drastically infection parameters such as virus accumulation, distribution and vector transmission. Sugar beet is an important crop that is frequently co-infected by the polerovirus beet chlorosis virus (BChV) and the closterovirus beet yellows virus (BYV), both vectored by the green peach aphid (Myzus persicae). These phloem-limited viruses are acquired while aphids ingest phloem sap from infected plants. Here we found that co-infection decreased transmission of BChV by ~50 %, but had no impact on BYV transmission. The drastic reduction of BChV transmission was not due to lower accumulation of BChV in co-infected plants, nor to reduced phloem sap ingestion by aphids from these plants. Using the SABER-FISH in situ hybridization technique on plants, we observed that 40 % of the infected phloem cells were co-infected and that co-infection caused redistribution of BYV in these cells. The BYV accumulation pattern changed from distinct intracellular spherical inclusions in mono-infected cells to a diffuse form in co-infected cells. There, BYV co-localized with BChV throughout the cytoplasm, indicative of virus-virus interactions. We propose that BYV-BChV interactions could restrict BChV access to the sieve tubes and reduce its accessibility for aphids and present a model of how co-infection could alter BChV intracellular movement and/or phloem loading and reduce BChV transmission.

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Vector acquisition and co-inoculation of two plant viruses influences transmission, infection, and replication in new hosts

Cited by 9 publications

References 91 publications

Emerging Themes and Approaches in Plant Virus Epidemiology

Emerging Themes and Approaches in Plant Virus Epidemiology

A New Perspective on the Co-Transmission of Plant Pathogens by Hemipterans

Interplay between a polerovirus and a closterovirus decreases aphid transmission of the polerovirus

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