Signaling at the Root Surface: The Role of Cutin Monomers in Mycorrhization

Most vascular plants interact with arbuscular mycorrhizal fungi (AMF) and are thereby provided significant advantages in nutrient acquisition, especially phosphate. The widespread retention of this symbiosis in vascular plants is testament to its importance and ancient origins. This highlight focuses on the reports of two of the first genes identified through forward genetic screens for AMF symbiotic mutants: Required for Abuscular Mycorrhization 1 (RAM1) and RAM2, which respectively encode a GRAS transcription factor and a glycerol-3-phosphate acyl-transferase (GPAT) that are required for the formation of fungal entry structures (hyphopodia) on the root surface. This provides the first insights into a mycorrhization specific signaling pathway and reveals cutin monomers as a critical component of signaling in the mycorrhizal symbiosis. We discuss the proposed links between these genes, and the role of cutin and its precursors in interactions with AMF, and oomycete and fungal pathogens. Root colonization by AMF involves the detection of compounds found in host root exudates such as strigolactones. Strigolactones are carotenoid-derived terpenoids that serve as a rhizosphere signal to activate responses in AMF, including hyphal branching, and thereby promote mycorrhizal colonization of the root surface. This involves the fungus making contact with the plant epidermal cell wall and forming a hyphopodium which is a lobed hyphal contact point with the root that serves as the entry point of the fungus into the epidermis. The hyphopodium is a specialized structure similar to, but distinct from, the pathogenic appressorium. The fungus then passes through an epidermal cell and colonizes the root cortex by extensive intercellular hyphal growth and the formation of terminal intracellular structures called arbuscules. The arbuscule, which serves as the nutrient exchange interface in the symbiosis, is highly branched and is surrounded by plant plasma membrane. It has been known for some time that the evolutionary history of the mycorrhizal symbioses is closely intertwined with that of a second root endosymbiosis called nodulation. The signaling required for the initiation of nodulation in legumes involves several genes that are also essential for mycorrhization (Kistner et al., 2005). This common set of genes is usually referred to as the common signaling pathway. For clarity, throughout this manuscript, common signally pathway genes identified in model legumes will be given as Medicago truncatula/Lotus japonicus. These shared components comprise a signaling circuit, which includes the ion channel DMI1 (Does not Make Infections)/POLLUX, DMI2/SYMRK (SYMbiosis Receptor like Kinase) and the calcium calmodulin kinase DMI3/CCaMK (Catoira et al., 2000) and its substrate IPD3 (Interacting Protein of DMI3)/Cyclops. Downstream of this shared signaling pathway lie the genes regulating the transcriptional outputs, including the GRAS transcription factors NSP1 and NSP2, which interact to regulate expression of nodulation genes (Hirsch et al., 2009).