Arbuscular mycorrhizal (AM) fungi influence the root system architecture of their hosts; however, the underlying mechanisms have not been fully elucidated. Ectomycorrhizal fungi influence root architecture via volatiles. To determine whether volatiles also play a role in root system changes in response to AM fungi, spores of the AM fungus Gigaspora margarita were inoculated on the same plate as either wild type (WT) Lotus japonicus, the L. japonicus mutant Ljcastor (which lacks the symbiotic cation channel CASTOR, which is required for inducing nuclear calcium spiking, which is necessary for symbiotic partner recognition), or Arabidopsis thaliana, separated by cellophane membranes (fungal exudates experiment), or on different media but with a shared head space (fungal volatiles experiment). Root development was monitored over time. Both germinating spore exudates (GSEs) and geminated-spore-emitted volatile organic compounds (GVCs) significantly promoted lateral root formation (LRF) in WT L. japonicus. LRF in Ljcastor was significantly enhanced in the presence of GVCs. GVCs stimulated LRF in A. thaliana, whereas GSEs showed an inhibitory effect. The expression profile of the genes involved in mycorrhizal establishment and root development were investigated using quantitative reverse transcription-PCR analysis. Only the expression of the LjCCD7 gene, an important component of the strigolactone synthesis pathway, was differentially expressed following exposure to GVCs. We conclude that volatile organic compounds released by the germinating AM fungal spores may stimulate LRF in a symbiosis signaling pathway (SYM)- and host-independent way, whereas GSEs stimulate LRF in a SYM- and host-dependent way.