Divide and Be Conquered—Cell Cycle Reactivation in Arbuscular Mycorrhizal Symbiosis

Arbuscular mycorrhizas (AM) are widespread symbiotic associations between 78% of vascular plant species globally and soil borne Glomeromycotina fungi. Analogous associations with fungi appeared over 400 million years ago and are thought to have played a major role in the transition of plants from aquatic to terrestrial environments. Indeed, extant AM fungi supply their host plants with water and mineral nutrients, resources that are as indispensable for them as they were for their earliest ancestors. AM development is a conserved process across extant host species with limited morphological variations in the symbiotic structures (Choi et al., 2018). Following an exchange of chemical signals (Zipfel and Oldroyd, 2017) root colonization starts with the formation of a hyphopodium on the root surface. Fungal entry in epidermal cells is anticipated by the assembly of the prepenetration apparatus (PPA), a broad, nucleus-associated cytoplasmic bridge. Here, exocytic and endocytic processes contribute to build a novel cell compartment, the symbiotic interface, hosting hyphae within an invagination of the plant cell membrane and a layer of unstructured cell wall components. Such symbiotic interfaces accommodate all intracellular hyphae as they develop toward the inner cortex, where their repeated branching originates arbuscules: the distinctive structures of this symbiosis, where mineral nutrients and water are transferred to the plant across the extensive periarbuscular interface, in exchange for sugars and lipids. The study of fungal accommodation has revealed that host cell rearrangement, calcium- mediated signals and major changes in gene expression extend to neighboring, uncolonized cells, indicating that signaling processes anticipate fungal development within the root tissues. In this context, we have recently shown that such prepenetration responses include cell cycle reactivation in cortical cells, with anticlinal cell divisions and recursive endoreduplication anticipating fungal colonization. We here propose a model depicting the recruitment of cell cycle processes as a strategy for arbuscule accommodation, speculating on its conservation in other, more recent, biotrophic interactions.