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

Abstract

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.

Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza in Petunia hybrida

“…4, Additional file 8). The MIG family was recently found in M. truncatula as a group of AM-induced genes with at least one member (MIG1) being required for arbuscule development [38]. The 11 MIG genes of petunia are distributed over 5 contigs in the genome (indicated by similar contig names in Fig.…”

“…4), i.e. some of them are arranged in close proximity in the genome, similar to the M. truncatula genes MIG1-MIG3 that are organized in a cluster as tandem repeats [38]. The MIG subfamily is specific to dicotyledonous plants species, but is absent from Arabidopsis (Additional file 8).…”

“…In particular, a dicot-specific clade that was recently described as the MIG clade [38] is highly induced in mycorrhizal roots.…”

Genome-wide survey and expression analyses of the GRAS gene family in Brassica napus reveals their roles in root development and stress response

“…To ensure the accuracy of our classification, we considered the current classification and gene functions of different species (Liu and Widmer 2014;Cenci and Rouard 2017;Niu et al 2017;Song et al 2017). As an SCLB member in M. truncatula was recently characterised and named MIG1 (Heck et al 2016), we renamed SCLB subfamily to MIG1.…”

Genome-Wide Characterization and Expression Profiling of Squamosa Promoter Binding Protein-Like (SBP) Transcription Factors in Wheat (Triticum aestivum L.)

“…A cotton v-myb avian myeloblastosis viral oncogene homolog (MYB) member, GbMYB5, is positively involved in plant adaptive responses to drought stress by activating the expression of dehydration-responsive genes in the abscisic acid (ABA)-dependent signaling pathway [4]. When activated by symbiotic arbuscular mycorrhizal fungi, GRAS (a plant-specific protein named after GAI, RGA and SCR) transcription factor Mycorrhiza-induced GRAS 1 (MIG1) is capable of modulating root cortex development by recruiting DELLA1 into the gibberellin (GA) signaling pathway as a transcriptional coactivator [5]. Additionally, the basic leucine zipper (bZIP) transcription factor LONG HYPOCOTYL 5 (HY5) plays a vital role in anthocyanin accumulation by regulating the expression of downstream anthocyanin biosynthesis genes in apple (Malus domestica) [6].…”