The Temporal Order of Mixed Viral Infections Matters: Common Events That Are Neglected in Plant Viral Diseases

Mixed infections of plant viruses are common in crops and represent a critical biotic factor with substantial epidemiological implications for plant viral diseases. Compared to single-virus infections, mixed infections arise from simultaneous or sequential infections, which can inevitably affect the ecology and evolution of the diseases. These infections can either exacerbate or ameliorate symptom severity, including virus-virus interactions within the same host that may influence a range of viral traits associated with disease emergence. This underscores the need for a more comprehensive understanding of how the order of virus arrival to the host can impact plant disease dynamics. From this perspective, we reviewed the current evidence regarding the impact of mixed infections within the framework of simultaneous and sequential infections in plants, considering the mode of viral transmission. We also examined how the temporal order of mixed infections could affect the dynamics of viral populations and present a case study of two aphid-transmitted viruses infecting melon plants, suggesting that the order of virus arrival significantly affects viral load and disease outcomes. Finally, we anticipate future research that reconciles molecular epidemiology and evolutionary ecology, underlining the importance of biotic interactions in shaping viral epidemiology and plant disease dynamics in agroecosystems.