Are transposons important facilitators of resistance evolution in the major agricultural pest fall armyworm?

Transposons are mobile selfish genetic elements that occur in the genomes of organisms across the tree of life. Once largely dismissed as ‘junk DNA’, there is growing recognition of their widespread evolutionary influence. This propensity emerges from the varied gene content of transposons and their frequent incorporation of host regulatory sequences, enhanced by their repetitiveness, replicative potential, modularity and mobility. It is now apparent that co-option of transposon sequences has provided key contributions to the evolution of diverse host traits, including pregnancy, memory, and immunity. Correspondingly, a major emerging question is, to what extent are transposons fundamental contributors to host evolution, and thus the diversity and complexity of life on Earth? To address this, it is necessary to move beyond consideration of individual cases of transposon co-option, towards systematic, genome-wide screens of transposon-host gene interactions. A topic of urgent applied relevance where transposon co-option is increasingly implicated, is resistance evolution. The evolution of resistance to treatment in parasites, pathogens, and pests is a major societal challenge, with vast implications for health, agriculture, and environment. The ongoing genomics revolution offers powerful new avenues for addressing this high-priority challenge, towards managing resistance and developing innovative solutions. For example, by elucidating the mechanistic processes underlying resistance evolution. Consequently, we propose a rigorous investigation into the role of transposons as under-appreciated facilitators of resistance evolution in eukaryotic pests, focusing on the major international agricultural pest, the fall armyworm moth (FAW, Spodoptera frugiperda). FAW is extremely generalist, causing significant damage to a huge variety of major crop plants, including staples such as maize, rice, wheat, and potatoes. FAW is also highly invasive and has spread around the world from an origin in South America, endangering livelihoods and food security, particularly among vulnerable smallholders across the developing world. These problems are compounded by rapid evolution of resistance to pesticides and transgenic plants in FAW. Working closely with industry, we propose three work packages to interrogate major outstanding questions on the influence of transposons in facilitating resistance evolution. Firstly, employing detailed comparative genomic analyses, we will assess transposon enrichment at FAW detoxification genes, the processes underlying observed patterns, and crucially, their functional relevance. We will also consider whether interactions among transposons and host detoxification genes contribute to the extreme host range of FAW and closely related species, which is a key facilitator of pestiferousness. Secondly, we will leverage the power of recently developed massively parallel reporter assays, to provide an exciting cutting-edge investigation into FAW gene regulatory landscapes, and the extent that transposons underlie regulatory evolution at detoxification genes, including increased expression. Thirdly, we will conduct a large-scale test of the influence of host physiological stress on transposon activity, a major outstanding hypothesis of general evolutionary relevance, with key resistance significance if chemical stress directly increases genetic variation in target organisms. Collectively, our proposal offers a novel and timely examination of a topic of fundamental evolutionary interest, coupled with high applied relevance for addressing major societal need, which may open new avenues for managing and combating resistance evolution. Thus, it is directly relevant to central priorities in both BBSRC’s high-level objectives ‘Rules of Life’ and ‘Sustainable Agriculture’. Meanwhile, our integral link with industry, and focus on a major pest of great consequence for global food security, aligns with UKRI-wide priorities to facilitate a secure and resilient world.