The impact of virus infection of a plant on an aphid’s behaviour has been observed in many studies [1]. Indeed, virus infection can alter plant biochemistry through the emission of volatile organic compounds and plant tissue content modification. These alterations can further impact the interactions between plants and aphids. However, although it is a well-known phenomenon, very few studies have explored the consequences of plant virus infection on the gene expression of aphids to understand better the aphid’s manipulation by the plant virus. In this context, the recommended study [2] reports a comprehensive transcriptomic analysis of the genes expressed by one aphid species, Myzus persicae, a vector of several plant viruses, when feeding on plants. Michelle Heck underlined how significant this study is for comprehending the molecular bases of aphid-vector manipulation by plant viruses (see below).

Interestingly, the study design has integrated several factors that might influence the gene expression of M. persicae when feeding on the plant. Indeed, the authors investigated the effect of two plant species (Arabidopsis thaliana and Camelia sativa) and two virus species [turnip yellows virus (TuYV) and cauliflower mosaic virus (CaMV)]. Noteworthy, the transmission mode of TuYV is circulative and persistent, while CaMV is transmitted by a semi-persistent non-circulative mode. As Juan José Lopez Moya mentioned, multiple comparisons allowed the identification of the different responses of aphids in front of different host plants infected or not by different viruses (see below). This publication is complementary to a previous publication from the same team focusing on plant transcriptome analysis [3].

Thanks to their experimental design, the authors identified genes commonly deregulated by both viruses and/or both plant species and deregulated genes by a single virus or a single plant. Figure 4 nicely summarizes the number of deregulated genes. A thorough discussion on the putative role of deregulated genes in different conditions gave a comprehensive follow-up of the results and their impact on the current knowledge of plant-virus-vector interactions.

This study has now opened the gate to promising research focusing on the functional validation of the identified genes while also narrowing the study from the body to the tissue level.

References:

1. Carr JP, Tungadi T, Donnelly R, Bravo-Cazar A, Rhee S-J, Watt LG, Mutuku JM, Wamonje FO, Murphy AM, Arinaitwe W, Pate AE, Cunniffe NJ, Gilligan CA (2020) Modelling and manipulation of aphid-mediated spread of non-persistently transmitted viruses. Virus Research, 277, 197845. https://doi.org/10.1016/j.virusres.2019.197845

2. Chesnais Q, Golyaev V, Velt A, Rustenholz C, Verdier M, Brault V, Pooggin MM, Drucker M (2022) Transcriptome responses of the aphid vector Myzus persicae are shaped by identities of the host plant and the virus. bioRxiv , 2022.07.18.500449, ver. 5 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.07.18.500449

3. Chesnais Q, Golyaev V, Velt A, Rustenholz C, Brault V, Pooggin MM, Drucker M (2022) Comparative Plant Transcriptome Profiling of Arabidopsis thaliana Col-0 and Camelina sativa var. Celine Infested with Myzus persicae Aphids Acquiring Circulative and Noncirculative Viruses Reveals Virus- and Plant-Specific Alterations Relevant to Aphid Feeding Behavior and Transmission. Microbiology Spectrum, 10, e00136-22. https://doi.org/10.1128/spectrum.00136-22

Zoonotic pathogens, those transmitted from animals to humans, constitute a major public health risk with high associated global economic costs. Diseases associated with these pathogens represent more than 60% of emerging infectious diseases and predominantly originate in wildlife (1). Over the last decades, the emergence and re-emergence of zoonotic pathogens have led to an increasing number of epidemics, as illustrated by the current Covid-19 pandemic. There is ample evidence that human impact on native ecosystems such as deforestation, agricultural development, and urbanization, is linked to spillover of pathogens from animals to humans (2). However, research and calls to action have mainly focused on the importance of surveillance and prevention of zoonotic emergences along landscape interfaces, with special emphasis on tropical forests and agroecosystems, and studies and reviews pointing out the zoonotic risk associated with cities are scarce.  Additionally, cities are sometimes wrongly seen as one homogeneous ecosystem, almost exclusively human, with a Northern hemisphere-biased perception of what a city is, which fails to take into account the ecological and socio-economic diversities that can constitute an urban area.

Here, Dobigny and Morand (3) aim to draw attention to the importance of urban ecosystems in zoonotic risk and advocate that further attention should be paid to urban, peri-urban and suburban areas. In this well-organized and well-documented review, the authors show, using updated literature, that cities are places where massive contacts occur between wildlife, domestic animals, and human inhabitants (thus constituting spillover opportunities), and that it is even likely that human and wildlife contact in urban centers is more prevalent than in wild areas, perhaps contrary to intuition. Indeed, cities currently constitute the most important environment of human life and are places for millions of close interactions between humans and animals, including pets and domestic animals, wild animals through the intrusion of wild urban-adapted species (e.g., some bat, rodent, or bird species among others), manipulation and consumption of wildlife meat, and the existence of wildlife meat markets, which all constitute a major risk for zoonotic spillover. In cities, lab escapees of zoonotic pathogens also exist, and trends of adaptation to urban ecological conditions of many vectors of primary health importance is also a concern. The authors further argue that cities are predominant places for both epidemic amplification of human-human transmitted pathogens, because they are places with high human densities and population growth, and for dissemination of reservoirs, vectors and pathogens, as they are transport hubs. Dobigny & Morand further predict, likely correctly, that cities may be important places for pathogen evolution.  Finally, they propose actions and recommendations to limit the risk of zoonotic spillover events from urban ecosystems and future directions for research aiming at assessing this risk. 

The reviewers found the manuscript well-organized and presented, timely, and bringing novel contributions to the field of zoonotic emergence. I strongly recommend this article, which should benefit a large audience, particularly in the context of the current Covid-19 pandemics and the ongoing One Health initiatives aiming at preventing future zoonotic disease emergence (4). 

References

(1) Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature, 451, 990–993. https://doi.org/10.1038/nature06536

(2) White RJ, Razgour O (2020) Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review, 50, 336–352. https://doi.org/10.1111/mam.12201

(3) Dobigny G, Morand S (2022) Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystems. Zenodo, 6444776, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6444776

(4) Morand S, Lajaunie C (2021) Biodiversity and COVID-19: A report and a long road ahead to avoid another pandemic. One Earth, 4, 920–923. https://doi.org/10.1016/j.oneear.2021.06.007