Network of GRAS Transcription Factors Involved in the Control of Arbuscule Development inLotus japonicus   

Abstract

(P.-M.D.) Arbuscular mycorrhizal (AM) fungi, in symbiosis with plants, facilitate acquisition of nutrients from the soil to their host. After penetration, intracellular hyphae form fine-branched structures in cortical cells termed arbuscules, representing the major site where bidirectional nutrient exchange takes place between the host plant and fungus. Transcriptional mechanisms underlying this cellular reprogramming are still poorly understood. GRAS proteins are an important family of transcriptional regulators in plants, named after the first three members: GIBBERELLIC ACID-INSENSITIVE, REPRESSOR of GAI, and SCARECROW. Here, we show that among 45 transcription factors up-regulated in mycorrhizal roots of the legume Lotus japonicus, expression of a unique GRAS protein particularly increases in arbuscule-containing cells under low phosphate conditions and displays a phylogenetic pattern characteristic of symbiotic genes. Allelic rad1 mutants display a strongly reduced number of arbuscules, which undergo accelerated degeneration. In further studies, two RAD1-interacting proteins were identified. One of them is the closest homolog of Medicago truncatula, REDUCED ARBUSCULAR MYCORRHIZATION1 (RAM1), which was reported to regulate a glycerol-3-phosphate acyl transferase that promotes cutin biosynthesis to enhance hyphopodia formation. As in M. truncatula, the L. japonicus ram1 mutant lines show compromised AM colonization and stunted arbuscules. Our findings provide, to our knowledge, new insight into the transcriptional program underlying the host's response to AM colonization and propose a function of GRAS transcription factors including RAD1 and RAM1 during arbuscule development.

Phosphate Treatment Strongly Inhibits New Arbuscule Development But Not the Maintenance of Arbuscule in Mycorrhizal Rice Roots

“…These data are in accordance with the "birdsfoot" arbuscules described by Gutjahr and Parniske (2013) Feddermann et al, 2010), RAM2 (Wang et al, 2012), VAMP72s (Ivanov et al, 2012), SYP132A (Pan et al, 2016), EXO70I (Zhang et al, 2015), VTI12 (Lota et al, 2013), ERF1 (Devers et al, 2013), RED (Groth et al, 2013;Gutjahr and Parniske, 2013), RAM1/ATA (Rich et al, 2015), RAD1 (Park et al, 2015;Xue et al, 2015), and FatM (Bravo et al, 2016). Hence, P inhibition may be related to the functions of these genes.…”

Crystal Structure of the GRAS Domain of SCARECROW-LIKE7 inOryza sativa

“…Moreover, GRAS proteins have been reported to form homodimers and heterodimers with other GRAS family members and this is likely important for their transcriptional regulation function (Itoh et al, 2002;Cui et al, 2007;Heo et al, 2011;Zhang et al, 2011;Gobbato et al, 2012;Murakami et al, 2013;Xue et al, 2015). Here, our structure of Os-SCL7 was determined in a dimer with helices A12, A79, and A69 at the dimer interface.…”

A Rice GRAS Gene Has an Impact on the Success of Arbuscular Mycorrhizal Colonization

“…They play important regulatory roles in a number of plant processes including signaling, development, abiotic stress, and symbiosis [22] [27]. Recent works demonstrated a direct involvement of several GRAS transcription factors in both mycorrhizal signaling and colonization, namely NSP1, NSP2, RAM1, DELLA, DELLA-interacting protein (DIP1) and RAD1 [15] Here, we focused on a rice GRAS protein previously identified by a whole transcriptome analysis as being specifically expressed in rice mycorrhizal roots and silent in response to mock treatment [34]. No further functional characterization of this GRAS protein, named OsAM18, is available so far.…”

“…The massive reorganization described in AM colonized plants requires a unique transcriptional program [7] which induces changes associated with metabolic pathways controlling nutritional exchanges, cell wall modifications, secondary metabolism, signal transduction, and protein turn-over [8]- [14]. On the basis of a RNAseq analysis, Xue and colleagues showed that 45 genes encoding transcriptional factors (TFs) or transcriptional regulators were significantly up-regulated in Lotus japonicus mycorrhizal roots when compared with non-mycorrhizal roots [15]. These genes belong to the main TFs families and include GRAS, AP2/ERF, NO APICAL MERISTEM, ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR, CUP-SHAPED COTYLEDON (NAC)-domain, MADS, MYB, C2H2 zinc finger, bZIP, ARF, WRKY DNA binding domain, NIN-like protein and LOB domain.…”

“…Other GRAS TFs, such as Required for Arbuscular Mycorrhization 1 (RAM1), Required for arbuscule development (RAD1) and DELLA protein, were recently identified in L. japonicus and Medicago truncatula. These genes have a functional role in arbuscule development [15] [18] [30]. The homologues of NSP1 and NSP2 have also been studied in rice, where at least 60 GRAS genes have been identified [31].…”