Translating virome analyses to support biosecurity, on-farm management, and crop breeding

Abstract

Virome analysis via high-throughput sequencing (HTS) allows rapid and massive virus identification and diagnoses, expanding our focus from individual samples to the ecological distribution of viruses in agroecological landscapes. Decreases in sequencing costs combined with technological advances, such as automation and robotics, allow for efficient processing and analysis of numerous samples in plant disease clinics, tissue culture laboratories, and breeding programs. There are many opportunities for translating virome analysis to support plant health. For example, virome analysis can be employed in the development of biosecurity strategies and policies, including the implementation of virome risk assessments to support regulation and reduce the movement of infected plant material. A challenge is to identify which new viruses discovered through HTS require regulation and which can be allowed to move in germplasm and trade. On-farm management strategies can incorporate information from high-throughput surveillance, monitoring for new and known viruses across scales, to rapidly identify important agricultural viruses and understand their abundance and spread. Virome indexing programs can be used to generate clean germplasm and seed, crucial for the maintenance of seed system production and health, particularly in vegetatively propagated crops such as roots, tubers, and bananas. Virome analysis in breeding programs can provide insight into virus expression levels by generating relative abundance data, aiding in breeding cultivars resistant, or at least tolerant, to viruses. The integration of network analysis and machine learning techniques can facilitate designing and implementing management strategies, using novel forms of information to provide a scalable, replicable, and practical approach to developing management strategies for viromes. In the long run, these management strategies will be designed by generating sequence databases and building on the foundation of pre-existing knowledge about virus taxonomy, distribution, and host range. In conclusion, virome analysis will support the early adoption and implementation of integrated control strategies, impacting global markets, reducing the risk of introducing novel viruses, and limiting virus spread. The effective translation of virome analysis depends on capacity building to make benefits available globally.

Keywords: crop breeding; microbiomes; pest management; phytosanitary standards; seed systems; surveillance; viromes.

Figure 1

Virome analysis reveals complex interactions in mixed and single infections, with impacts from global to local scales. Translating information at each scale has both important potential as well as challenges for implementation. Effective translation can improve on-farm management, crop breeding and seed systems, and phytosanitary activities.

Figure 2

The spatial resolution of virome analysis, from low-resolution (counties and farms) to high-resolution (hosts), and virus associations at each scale. (A) Geographic representation of counties in a region, farms within a county, and hosts within a farm. Each layer could contain a different subset of viruses (a different virome). (B) Bipartite networks representing associations between two types of nodes, where circles represent viruses (v1 to v4), and where evaluation can be at multiple scales, for example: by region, where squares represent counties (i, j, k), by farm, where squares represent plots (1 to 4), and by host, where squares represent individual plants (a to e). (C) A one-mode network, where links between viruses represent their shared geographic or host associations and links between locations indicate similarity of their viromes, by region or by farm. Links between hosts represent similar viromes.

Figure 3

Left: Characteristic leaf symptoms of cassava mosaic disease (CMD), a disease associated with 12 different species of begomoviruses, affecting cassava in Africa, East Asia and Southeast Asia (Legg et al., 2015). Center: Cassava plant in Southeast Asia showing mixed symptoms of CMD (caused by Sri Lankan cassava mosaic virus) and cassava witches’ broom disease, a co-infection common in the region (Siriwan et al., 2020). Right: Leaf and root symptoms of cassava frogskin disease associated with a unique virome from the Americas (Pardo et al., 2022). Photos: W. Cuellar.

Figure 4

Virome management units associated with maize lethal necrosis, as described below.

Figure 5

Thirty-two countries requested germplasm material for potato, sweetpotato, and Andean roots and tubers in 2020 from the Genebank of the International Potato Center (CIP) in Lima, Peru (data retrieved from https://cipotato.org/genebankcip/process/distribution_acquisition/). Virome analysis can help to ensure that viruses that may endanger crop production are not present in germplasm.