Unequal requirement of KAI2 for AM symbiosis across angiosperms

Development of arbuscular mycorrhiza (AM), a symbiosis between plants and beneficial Glomeromycotan fungi, is largely under plant control. Several genes, required for AM development, are proposed to be regulated by the karrikin signalling module, comprising the alpha/beta hydrolase receptor KARRIKIN INSENSITIVE 2 (KAI2), the F-box protein MORE AXILLARY GROWTH2 (MAX2) and the transcriptional repressor SUPPRESSOR OF MAX2 1 (SMAX1), which is ubiquitylated for proteasomal degradation upon KAI2-ligand-induced binding to the KAI2-MAX2 complex. Rice and Brachypodium distachyon kai2 mutants are incapable of forming AM. Here, we show that in Lotus japonicus, Pisum sativum, and Nicotiana benthamiana, KAI2 only quantitatively affects AM development, indicating angiosperms vary in their requirement for KAI2-signalling to support AM. Comparative transcriptomics of L. japonicus and B. distachyon roots after treatment with fungal signalling molecules revealed some AM-relevant genes respond KAI2-independently in L. japonicus but not in B. distachyon. Consistently we obtained evidence for low-level degradation of SMAX1 in Ljkai2a,b observed through a ratiometric reporter for the SMAX1 degron (SMAX1D2). Further, we found an unexpected accumulation of SMAX1D2 in in response to AM even in wild type. Together, this suggests an unexpected role of SMAX1 accumulation in AM roots and that in AM symbiosis of L. japonicus, redundant mechanisms drive SMAX1 degradation and gene activation independently of KAI2.