Physiological and transcriptomic response of Medicago truncatula to high and low benefit mycorrhizal fungi

Arbuscular mycorrhizal (AM) fungi provide their host plants with greater access to limited mineral nutrients, but the amount they provide can be variable. Here, we evaluated the capacity of the high-benefit fungus Rhizophagus irregularis 09 and the low-benefit fungus Glomus aggregatum 165 to transfer nitrogen and phosphorus to the host plant Medicago truncatula, and identified putative molecular mechanisms regulating the physiological response of the host to these fungi. R. irregularis led to an increase in plant biomass and transferred more nitrogen and phosphate to the host than G. aggregatum. This increase was linked to elevated expression of known mycorrhiza-induced phosphate (PT8), ammonium (AMT2;3), and nitrate (NPF4.12) transporters in the roots, as well as the putative ammonium transporter NIP1;5. R. irregularis also stimulated the expression of photosynthesis related genes in the shoot and the upregulation of the mycorrhiza-induced sugar transporter SWEET1.2 and the lipid biosynthesis gene RAM2 in the roots, which is indicative of increased carbon flux to this fungus. In contrast, G. aggregatum induced biotic stress defense response genes (e.g., Medtr4g120760 and Medtr8g096900) in the shoots, and several genes associated with the GO term "response to water deprivation" in the roots of M. truncatula. This could indicate that the host perceives colonization by the low-benefit fungus as pathogen attack, or that G. aggregatum is more effective than R. irregularis at priming host defense responses. Our findings reveal novel insights into the molecular mechanisms by which host plants reward high-but sanction low-benefit arbuscular mycorrhizal symbionts. One sentence summaryColonization with high- and low-benefit arbuscular mycorrhizal fungi leads to distinct physiological and transcriptomic changes in the roots and shoots of Medicago truncatula.