It is argued that endosymbionts are often a key component of the selective environment experienced by vectors and viruses and hypothesize that they may play important roles in modulating the direction and magnitude of virus‐induced effects on plant–insect interactions.
Abstract
Insect‐vectored plant viruses frequently alter plant–insect interactions in ways favourable to their own transmission (often referred to as manipulation).
Variation in virus‐induced effects is often attributed to genetic variability and local adaptation in virus and host‐plant populations, but emerging evidence suggests that vector‐associated microbial symbionts may also play important roles.
Vector insects harbour both obligate and facultative endosymbionts that can strongly influence vector traits and their interactions with host plants. Yet relatively few studies to date have examined how endosymbionts influence virus effects on plant–insect interactions and transmission.
We argue that endosymbionts are often a key component of the selective environment experienced by vectors and viruses and hypothesize that they may play important roles in modulating the direction and magnitude of virus‐induced effects on plant–insect interactions.
We outline key questions and priorities for research that will integrate virus–endosymbiont interactions into disease ecology. Such integration is crucial for understanding the evolution and ecology of viral and endosymbiont effects on vector biology, as well as the implications for disease transmission in agricultural and natural systems.
Plant viruses are evolutionarily endowed with traits that enhance their survival and dissemination attributes both in host plants and insect vectors. This review highlights current understanding of these multifaceted interactions, positioning plant viruses as master regulators of the intricate tripartite interactions. Direct viral effects on vector physiology and behaviour, highlighting evidence that viral infection may contribute to changes in olfactory systems, epigenetic modifications, involvement of salivary effectors, and horizontal gene transfer events that may vary vector competence, were summarised. The indirect mechanisms mediated through virus-induced alterations in host plant responses, including changes in volatile emissions, the development of visually and chemically attractive symptoms, and modulation of host immune defences that may influence vector attraction and feeding behaviour, were discussed. These viral infections have profound ecological and agricultural consequences, reflecting the fine balance these pathogens maintain between preserving host viability and maximising transmission. In intensively managed agro-ecosystems, environmental and biological conditions can strengthen these interactions, potentially promoting epidemic spread and altering vector behaviour. Deciphering these evolutionary strategies deepens our understanding of the dynamics governing pathogen-host-vector systems and opens new possibilities for designing targeted, sustainable interventions to disrupt viral transmission in crops.
P. Kaur, Abhisha Roy, Saikat Bhattacharjee et al.· Plant, Cell and Environment· 0 citations
With the advance of metatranscriptomic sequencing, an increasing number of symbiotic viruses have been recognized in insects. These insect symbiotic viruses not only modulate key aspects of insect biology, including physiology, fecundity, development, and behavior, but also influence the vector competence of arthropods for transmitting arboviruses. The majority of such vectors belong to the orders Hemiptera and Diptera, which transmit a wide spectrum of plant and animal arboviruses. Although insect symbiotic viruses usually replicate exclusively within insect cells, several symbiotic viruses have also been detected in insect secretions and even in host plants, indicating they may have more profound functions than we originally thought. In this review, we synthesize current knowledges on the hidden roles of insect symbiotic viruses across three key dimensions: their impact on insect adaptation to host plants, as reflected in fitness, feeding behavior, dispersal capacity, and resistance traits; their regulation of vector competence for the transmission of both plant and animal arboviruses; and their emerging application as biotechnological tools for the delivery of double-stranded RNA (dsRNA), small interfering RNA (siRNA), or recombinant proteins to control viral diseases in agriculture and public health.
Hong Lu, Yumei Fu, Jiahui Tong et al.· Current Opinion in Insect Sc...· 0 citations
Plant rhabdoviruses comprise a group of economically important pathogens that exhibit a complex dual-host infection cycle across plants and insect vectors, relying on exquisitely adapted cross-kingdom infection and survival strategies. In this review, we summarize recent advances in understanding plant rhabdovirus-host interactions, with a focus on the molecular basis underlying viral manipulation of host functions. We highlight key host factors or subcellular structures hijacked by plant rhabdoviruses to support robust viral replication and intracellular transport. We further explore the diverse counter-defense mechanisms deployed by plant rhabdoviruses to evade or suppress host immunity, including RNA silencing, phytohormone signaling cascades, and autophagy-mediated degradation. Finally, we discuss the intimate insect-virus interfaces, detailing how viral effectors modulate vector feeding behaviors, physiology, and innate immune responses to facilitate persistent, propagative transmission. Collectively, these advances establish an integrated framework for understanding the cross-kingdom pathogenesis of plant rhabdoviruses and provide insights for developing innovative crop protection strategies.
Kaili Wu, Wenlin Yang, Zhenghe Li· Current Opinion in Virology· 0 citations
This review summarizes recent progress in elucidating plant virus-vector molecular interactions and their potential use in innovative strategies for virus and vector control.
B. Bonning· Current Opinion in Virology· 0 citations
Plant responses to insect feeding mediate interactions with other community members and may influence community assembly on the induced plant. Since plants perceive herbivory through damage patterns and salivary components, changes in these herbivore traits, such as caused by parasitism, may alter herbivore‐induced plant‐mediated interactions.
Upon parasitism, many parasitoids inject a combination of polydnavirus and venom into their host. In doing so, the host's behaviour and physiology are modified. The injection of polydnavirus has been identified as a prominent driver of plant‐mediated interactions initiated by parasitised herbivores. However, most evidence for such plant‐mediated effects comes from greenhouse or laboratory studies.
We investigated the ecological consequences of parasitism and its associated injection components on assembly of arthropod communities in an open‐field setting. We exposed wild
Brassica oleracea
plants to herbivory by unparasitised
Pieris brassicae
caterpillars, caterpillars parasitised by
Cotesia glomerata
, caterpillars injected with polydnavirus and/or venom, and we used uninduced plants as control. We monitored the naturally occurring arthropod community on these plants throughout the growing season, focusing on both overall community composition and the abundance of individual species.
Arthropod community composition was marginally affected by components of parasitism and subtle effects were found for interactions with specific herbivore species. Plants damaged by
P. brassicae
injected with both polydnavirus and venom were colonised more often by
Mamestra brassicae
caterpillars,
Myzus persicae
aphids and aphid parasitoids compared to uninduced plants or plants induced by unparasitised
P. brassicae
caterpillars.
Our results show that parasitoid polydnavirus and venom, either alone or in combination, affect colonisation by members of the arthropod community in a natural field setting. These modulating effects deserve attention in future studies that investigate the dynamics of plant‐arthropod communities.
Sarah N. Kalisvaart, Gabriele Bolletta, Gabriel Joachim et al.· Ecological Entomology· 0 citations
BACKGROUND
Plant viruses have evolved adaptations that enable them to alter host cues, thereby facilitating their replication and efficient transmission by insect vectors. Satellite RNAs (satRNAs), which accompany certain plant RNA viruses and are dependent on them for replication and transmission, can change the progression of pathogenesis and the expression of disease symptoms. This study aimed to analyse how the change in the course of infection by satRNA (exacerbation or mitigation of pathogenesis) impacts the subsequent stages of virus transmission. We hypothesised that satRNAs influence insect behaviour toward infected plants depending on their effect on pathogenesis progress; specifically, a significant disease exacerbation reduces plant attractiveness to aphids, whereas symptom mitigation promotes attraction.
RESULTS
Using peanut stunt virus (PSV) and cucumber mosaic virus (CMV), and their satRNAs, which induce divergent infection symptoms on Nicotiana benthamiana or Solanum lycopersicum plants, olfactometry, electrical penetration graph (EPG) monitoring, virus acquisition and transmission by Myzus persicae were analysed. The results showed that satRNA, naturally associated with the helper virus, that alleviate disease symptoms caused the plants to be more attractive to the insect vectors. On the other hand, the presence of satRNAs leading to symptom exacerbation reduced plant attractiveness and discouraged phloem feeding. However, acquisition effects were host-dependent: while symptom-exacerbating satRNAs generally reduced acquisition, nc-satRNA markedly enhanced CMV acquisition from N. benthamiana. Moreover, virus transmission was significantly reduced only in S. lycopersicum.
CONCLUSIONS
These findings suggest that symptom-attenuating satRNAs have greater capacity to persist in the environment by limiting disease damage in host plants and maintaining plant attractiveness to aphid vectors, thereby facilitating virus acquisition and transmission. In contrast, symptom-exacerbating satRNA variants appear not only to diminish the number of cells available for viral replication due to severe symptoms but also to reduce plant palatability and to impair vector feeding and thus virus transmission, particularly in crop hosts such as S. lycopersicum, which may limit their environmental persistence. Together, these results underscore the epidemiological relevance of satRNA-mediated symptom modulation as a factor shaping virus spread in natural and agricultural settings.
Barbara Wrzesińska-Krupa, Patryk Frąckowiak, M. Budziszewska et al.· BMC Plant Biology· 0 citations