Root cortex development is fine-tuned by the interplay of MIGs, SCL3 and DELLAs during arbuscular mycorrhizal symbiosis.

Root development is a crucial process that determines the ability of plants to acquire nutrients, adapt to the substrate and withstand changing environmental conditions. Root plasticity is controlled by a plethora of transcriptional regulators that allow, in contrast to tissue development in animals, post-embryonic changes that give rise to new tissue and specialized cells. One of these changes is the accommodation in the cortex of hyperbranched hyphae of symbiotic arbuscular mycorrhizal (AM) fungi, called arbuscules. Arbuscule-containing cells undergo massive reprogramming to coordinate developmental changes with transport processes. Here we describe a novel negative regulator of arbuscule development, MIG3. MIG3 induces and interacts with SCL3, both of which modulate the activity of the central regulator DELLA, restraining cortical cell growth. As in a tug-of-war, MIG3-SCL3 antagonizes the function of the complex MIG1-DELLA, which promotes the cell expansion required for arbuscule development, adjusting cell size during the dynamic processes of the arbuscule life cycle. Our results in the legume plant Medicago truncatula advance the knowledge of root development in dicot plants, showing the existence of additional regulatory elements not present in Arabidopsis that fine-tune the activity of conserved central modules.

Symbiotic Fungi Control Plant Root Cortex Development through the Novel GRAS Transcription Factor MIG1.

In an approaching scenario of soil nutrient depletion, root association with soil microorganisms can be key for plant health and sustainability [1-3]. Symbiotic arbuscular mycorrhizal (AM) fungi are major players in helping plants growing under nutrient starvation conditions. They provide plants with minerals like phosphate and, furthermore, act as modulators of plant growth altering the root developmental program [4, 5]. However, the precise mechanisms involved in this latter process are not well understood. Here, we show that AM fungi are able to modulate root cortex development in Medicago truncatula by activating a novel GRAS-domain transcription factor, MIG1, that determines the size of cortical root cells. MIG1 expression peaks in arbuscule-containing cells, suggesting a role in cell remodeling during fungal accommodation. Roots ectopically expressing MIG1 become thicker due to an increase in the number and width of cortical cells. This phenotype is fully counteracted by gibberellin (GA) and phenocopied with a GA biosynthesis inhibitor or by expression of a dominant DELLA (Δ18DELLA1) protein. MIG1 downregulation leads to malformed arbuscules, a phenotype rescued by Δ18DELLA1, suggesting that MIG1 intersects with the GA signaling to control cell morphogenesis through DELLA1. DELLA1 was shown to be a central node controlling arbuscule branching [6-8]. Now we provide evidence that, together with MIG1, DELLA1 is responsible for radial cortical cell expansion during arbuscule development. Our data point toward DELLA proteins being not only longitudinal root growth repressors [9] but also positive regulators of cortical radial cell expansion, extending the knowledge of how DELLAs control root growth.