Unraveling Cross-Kingdom Interactions Among Plants, Mycorrhizal Fungi, and Bacteria: Current Insights and Future Directions

Xiaoli Yu¹Mingfei Chen²Yuguo Yang²Huang Yu³Ruiwen Hu^4*

• ¹Southern Marine Science and Engineering Guangdong Laboratory - Zhuhai, Zhuhai, China
• ²E O Lawrence Berkeley National Laboratory, Berkeley, United States
• ³University of South China, Hengyang, China
• ⁴Division of Environmental Genomics and Systems Biology, Berkeley Lab (DOE), Berkeley, United States

). Elucidating the mechanisms underlying these cross-kingdom interactions is essential for harnessing microbial functions to enhance plant tolerance to environmental stresses, improve agricultural productivity, and mitigate the impacts of climate change. Recent research has highlighted several major mechanisms governing plant-fungi-bacteria interactions, including chemical signaling via root exudates and volatile organic compounds, nutrient exchange and recycling among partners, and cooperative defense against pathogens (Sasse et al., 2018, Camargo et al., 2023, Jansson et al., 2023, Razo-Belmán et al., 2023, Yang et al., 2024). Root exudates (e.g., flavonoids, siderophores, terpenes) are now recognized as key regulators of plant-microbe communication, shaping microbial recruitment and influencing plant performance (Fan et al., 2025). However, the majority of root exudate compounds remain structurally and functionally uncharacterized, limiting a comprehensive understanding of their ecological and evolutionary significance. Symbioses between plants and arbuscular mycorrhizal fungi (AMF) provide another key example of microbe-mediated nutrient exchange, particularly in nitrogen and phosphorus acquisition (Bennett et al., 2022). Beyond the rhizosphere, the hyphosphere (i.e., the microenvironment surrounding AMF hyphae), provides an interface for plant-AMF-bacteria interactions (Duan et al., 2024). Yet, the ecological roles of hyphosphere-associated bacteria and their contribution to AMF functionality remain poorly understood. Traditional approaches to studying plant-microbe interactions have often relied on multi-omics analyses or the characterization of individual microbial strains. By contrast, synthetic ecology offers an alternative framework for studying these interactions by enabling researchers to investigate the complex dynamics and functional contributions of specific microbial consortia in relation to plant health and growth. For example, synthetic microbial communities (SynComs) composed of aluminum-tolerant bacterial strains isolated from the rice rhizosphere have been shown to alleviate aluminum toxicity and enhance rice yield (Liu et al., 2023). Despite these advances, major challenges remain for SynCom-based strategies, including the rational selection of functionally complementary strains, optimization of community composition, and prediction of long-term ecological stability under field conditions. Overall, substantial progress has been made in understanding the mechanistic bases of plant-microbe interactions. Nevertheless, critical knowledge gaps remain, particularly regarding the chemical diversity of root exudates, the roles of bacteria in the hyphosphere, and the ecological predictability of engineered SynComs.To address these knowledge gaps, our Research Topic titled "The Complex Cross-Kingdom Interactions Between Plant, Mycorrhizal Fungi and Bacteria: Current These studies collectively highlight the intricate and essential role of cross-kingdom interactions in regulating plant health and ecosystem processes, while also offering new perspectives for advancing microbiome engineering toward sustainable agriculture. Building on these insights, we propose several priorities for future research: First, molecular and systems-level approaches should be systematically employed to unravel the molecular mechanisms underlying plant-mycorrhizal fungi-bacteria interactions, with particular emphasis on signaling cascades and metabolite exchange that mediate inter-kingdom communication.Second, it is critical to determine how such plant-microbe associations respond to global change drivers, including climate variability, environmental pollution, and diverse environmental stresses. Finally, long-term experimental and field-based approaches are needed to evaluate microbiome engineering strategies and to enable robust assessments of their impacts on plant performance, ecosystem stability, and resilience.