LACK OF SYMBIONT ACCOMMODATION controls intracellular symbiont accommodation in root nodule and arbuscular mycorrhizal symbiosis in Lotus japonicus

Nitrogen-fixing rhizobia and arbuscular mycorrhizal fungi (AMF) form symbioses with plant roots and these are established by precise regulation of symbiont accommodation within host plant cells. In model legumes such as Lotus japonicus and Medicago truncatula, rhizobia enter into roots through an intracellular invasion system that depends on the formation of a root-hair infection thread (IT). While IT-mediated intracellular rhizobia invasion is thought to be the most evolutionarily derived invasion system, some studies have indicated that a basal intercellular invasion system can replace it when some nodulation-related factors are genetically modified. In addition, intracellular rhizobia accommodation is suggested to have a similar mechanism as AMF accommodation. Nevertheless, our understanding of the underlying genetic mechanisms is incomplete. Here we identify a L. japonicus nodulation-deficient mutant, with a mutation in the LACK OF SYMBIONT ACCOMMODATION (LAN) gene, in which root-hair IT formation is strongly reduced, but intercellular rhizobial invasion eventually results in functional nodule formation. LjLAN encodes a protein that is homologous to Arabidopsis MEDIATOR 2/29/32 possibly acting as a subunit of a Mediator complex, a multiprotein complex required for gene transcription. We also show that LjLAN acts in parallel with a signaling pathway including LjCYCLOPS. In addition, the lan mutation drastically reduces the colonization levels of AMF. Taken together, our data provide a new factor that has a common role in symbiont accommodation process during root nodule and AM symbiosis. Author summary Symbiosis between plants and beneficial microbes such as nitrogen-fixing bacteria and arbuscular mycorrhizal fungi has enabled plant colonization of new environments. Root nodule symbiosis with nitrogen-fixing rhizobia enables sessile plants to survive in a nitrogen-deficient environment. To establish the symbiosis, host plant cells need to accommodate rhizobia during nodule development, a process mediated by a plant-derived intracellular structure called the infection thread (IT). In this study, we show that LACK OF SYMBIONT ACCOMMODATION (LAN) is involved in intracellular rhizobia accommodation in the model leguminous plant Lotus japonicus. LjLAN encodes a putative subunit of Mediator complex, a multiprotein complex that has a fundamental role as an activator of gene transcription. Mutation analysis suggests that LjLAN is required for root hair IT formation, which enables swift and efficient rhizobial accommodation. Moreover, we show that LjLAN is required for symbiosis with arbuscular mycorrhizal fungi. These data add a new component to the molecular mechanism relevant to the establishment of root nodule and arbuscular mycorrhizal symbiosis.