Arbuscular mycorrhizal fungal community abundance, functions, and symbiotic interactions revealed by root metatranscriptomes

Abstract Arbuscular mycorrhizal (AM) fungal communities are often profiled by metabarcoding, but this approach can bias abundance estimates and provide limited insight into community function and interactions with the host. Here, using weekly, field‐based multi‐omics, we find metatranscriptomes and metagenomes increase estimates of AM fungal relative abundance 6−15‐fold over rDNA metabarcoding and that root AM fungal relative abundance correlates strongly with sorghum forage yield ( R > 0.9) and moderately with grain yield/quality. AM fungal relative abundance is impacted directly by sorghum development and indirectly by drought via suppressed sorghum fatty acid gene expression. Gene co‐expression network revealed coordinated plant and AM fungal functions in structural reorganization, resource exchange, and signal communication between the symbiotic partners. We found that early‐season co‐transcriptions of AM fungal and host genes feature cytoskeletal genes essential for arbuscule formation, the fungal‐plant organs of nutrient and mineral exchange. Late‐season plants downregulate cytoskeletal genes, but AM fungi continue their upregulation, which is associated with fungal sporulation and putative mating. Our study identifies previously ignored massive underestimation of AM fungal relative abundance, highlights the predictive role of AM fungal relative abundance for crop productivity, and uncovers symbiotic life history dynamics underpinned by coupled and decoupled co‐expression of plant and AM fungal genes.