An Autophagy-Related Kinase Is Essential for the Symbiotic Relationship between <i>Phaseolus vulgaris</i> and Both Rhizobia and Arbuscular Mycorrhizal Fungi

Abstract

Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and <i>Saccharomyces cerevisiae</i>, only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean (<i>Phaseolus vulgaris</i>) <i>PI3K</i> severely impaired symbiosis in composite <i>P. vulgaris</i> plants with endosymbionts such as <i>Rhizobium tropici</i> and <i>Rhizophagus irregularis</i> Downregulation of Pv<i>-PI3K</i> was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAi-mediated downregulation of one of these genes, <i>Beclin1</i>/<i>Atg6</i>, resulted in a similar phenotype as observed for transgenic roots in which Pv<i>-PI3K</i> had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of <i>P. vulgaris</i> with beneficial microorganisms.