Plant viruses and the microbiome: a complex network shaping plant health and disease resistance

Plant viruses and microbiomes are pivotal to plant health, growth, and their ability to withstand environmental challenges. However, the extent to which viruses engage in direct or indirect crosstalk with plant-associated microbial communities remains largely unexplored. Traditionally, plant viruses are considered as harmful agents that disrupt normal plant functions, but new research indicates they may also engage in complex interactions with the plant's microbiome. On the other hand, the plant microbiome, comprising a diverse assembly of bacteria, fungi, and other microbes, can influence the plant's responses to viral infections, potentially altering the course of the disease. Thus, we emphasize the intricate interplay between plant viruses and microbiomes, particularly how viruses might "communicate" with microbial communities to alter the host environment or bypass immune defenses. The mechanisms driving these interactions, such as virus-induced shifts in plant metabolism, signaling pathways, and immune responses that indirectly affect microbiome composition are also discussed. The beneficial effect of plant-associated microbial communities against viral infections and the strategy of microbiome-based approaches for managing viral diseases are also focused. By moving beyond the traditional view of pathogen-host interactions, this review will highlight the importance of considering the three-way relationship among plants, viruses, and microbiomes to advance our understanding of plant health and foster innovative solutions for sustainable agriculture.