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The arbuscular mycorrhizal fungi (AMFs) are obligate root symbionts in the subphylum Glomeromycotina that can benefit land plants by increasing their soil nutrient uptake in exchange for photosynthetically fixed carbon sources. To date, annotated genome data from representatives of the AMF orders Glomerales, Diversisporales and Archaeosporales have shown that these organisms have large and highly repeated genomes, and no genes to produce sugars and fatty acids. This led to the hypothesis that the most recent common ancestor (MRCA) of Glomeromycotina was fully dependent on plants for nutrition. Here, we aimed to further test this hypothesis by obtaining annotated genome data from a member of the early diverging order Paraglomerales ( Paraglomus occultum ). Genome analyses showed this species carries a 39.6 Mb genome and considerably fewer genes and repeats compared to most AMF relatives with annotated genomes. Consistent with phylogenies based on ribosomal genes, our phylogenetic analyses suggest P. occultum as the earliest diverged branch within Glomeromycotina. Overall, our analyses support the view that the MRCA of Glomeromycotina carried hallmarks of obligate plant biotrophy. The small genome size and content of P. occultum could either reflect adaptive reductive processes affecting some early AMF lineages, or indicate that the high gene and repeat family diversity thought to drive AMF adaptability to host and environmental change was not an ancestral feature of these prominent plant symbionts. 

Summary That arbuscular mycorrhizal (AM) fungi covary with plant communities is clear, and many papers report nonrandom associations between symbiotic partners. However, these studies do not test the causal relationship, or ‘codependency’, whereby the composition of one guild affects the composition of the other. Here we outline underlying requirements for codependency, compare important drivers for both plant and AM fungal communities, and assess how host preference – a pre‐requisite for codependency – changes across spatiotemporal scales and taxonomic resolution for both plants and AM fungi. We find few examples in the literature designed to test for codependency and those that do have been conducted within plots or mesocosms. Also, while plants and AM fungi respond similarly to coarse environmental filters, most variation remains unexplained, with host identity explaining less than 30% of the variation in AM fungal communities. These results combined question the likelihood of predictable co‐occurrence, and therefore evolution of codependency, between plant and AM fungal taxa across locations. We argue that codependency is most likely to occur in homogeneous environments where specific plant – AM fungal pairings have functional consequences for the symbiosis. We end by outlining critical aspects to consider moving forward.