The Petunia GRAS Transcription Factor ATA/RAM1 Regulates Symbiotic Gene Expression and Fungal Morphogenesis in Arbuscular Mycorrhiza

Rich, Mélanie K.; Schorderet, Martine; Bapaume, Laure; Falquet, Laurent; Morel, Patrice; Vandenbussche, Michiel; Reinhardt, Didier

doi:10.1104/pp.15.00310

Cited by 58 publications

(68 citation statements)

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“…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.…”

Section: The Potential Mechanism Of P Inhibitionsupporting

confidence: 73%

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

et al. 2016

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ORCID IDs: 0000-0002-9997-490X (Y.K.); 0000-0001-8867-5085 (C.S.).Phosphorus (P) is a crucial nutrient for plant growth, but its availability to roots is limited in soil. Arbuscular mycorrhizal (AM) symbiosis is a promising strategy for improving plant P acquisition. However, P fertilizer reduces fungal colonization (P inhibition) and compromises mycorrhizal P uptake, warranting studies on the mechanistic basis of P inhibition. In this study, early morphological changes in P inhibition were identified in rice (Oryza sativa) using fungal cell wall staining and live-cell imaging of plant membranes that were associated with arbuscule life cycles. Arbuscule density decreased, and aberrant hyphal branching was observed in roots at 5 h after P treatment. Although new arbuscule development was severely inhibited, preformed arbuscules remained intact and longevity remained constant. P inhibition was accelerated in the rice pt11-1 mutant, which lacks P uptake from arbuscule branches, suggesting that mature arbuscules are stabilized by the symbiotic P transporter under high P condition. Moreover, P treatment led to increases in the number of vesicles, in which lipid droplets accumulated and then decreased within a few days. The development of new arbuscules resumed within by 2 d. Our data established that P strongly and temporarily inhibits new arbuscule development, but not intraradical accommodation of AM fungi.

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Section: The Potential Mechanism Of P Inhibitionsupporting

confidence: 73%

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

et al. 2016

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“…The mycorrhizal phenotype reported for ram1-1 included a defect in hyphopodium formation and substantially reduced colonization but wild-type arbuscules, whereas ram1-2 showed small, undeveloped arbuscules (Gobbato et al, , 2013. Recent reports of ram1 mutants of L. japonicus and P. hybrida noted low colonization and the presence of malformed arbuscules (Rich et al, 2015;Xue et al, 2015).…”

Section: Ram 1-3 Is Unable To Support Arbuscule Branchingmentioning

confidence: 95%

“…So far, transcription factors required for AM symbiosis include CYCLOPS (Yano et al, 2008), DELLAs (Floss et al, 2013;Foo et al, 2013;Yu et al, 2014;Takeda et al, 2015), Reduced Arbuscular Mycorrhiza1 (RAM1; Gobbato et al, 2012;Rich et al, 2015;Xue et al, 2015), Required for Arbuscule Development1 (RAD1; Xue et al, 2015), MtERF1 (Devers et al, 2013), and DELLA-Interacting Protein1 (DIP1; Yu et al, 2014). Among these transcriptional regulators, DELLAs, RAM1, RAD1, and DIP1 belong to the GRAS (for GA 3 insensitive [GAI], Repressor of GAI [RGA], and Scarecrow [SCR]) family, a large, plantspecific gene family with members that regulate transcription and influence several aspects of plant development, including root development (Bolle, 2004).…”

mentioning

confidence: 99%

“…However, subsequently, it was noted that arbuscules in ram1 were small, suggesting a potential role for RAM1 in arbuscule development (Gobbato et al, 2013). Recent analyses of ram1 mutants in Lotus japonicus and Petunia hybrida show that RAM1 is required to support wildtype arbuscule development (Rich et al, 2015;Xue et al, 2015). In L. japonicus, a second GRAS factor RAD1 interacts with RAM1, and rad1 mutants showed a high proportion of small, degenerated arbuscules, suggesting a requirement for RAD1 in maintenance of the symbiosis (Xue et al, 2015).…”

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confidence: 99%

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Hyphal branching during arbuscule development requires RAM1

et al. 2015

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During arbuscular mycorrhizal symbiosis, arbuscule development in the root cortical cell and simultaneous deposition of the plant periarbuscular membrane generate the interface for symbiotic nutrient exchange. The transcriptional changes that accompany arbuscule development are extensive and well documented. By contrast, the transcriptional regulators that control these programs are largely unknown. Here, we provide a detailed characterization of an insertion allele of Medicago truncatula Reduced Arbuscular Mycorrhiza1 (RAM1), ram1-3, which reveals that RAM1 is not necessary to enable hyphopodium formation or hyphal entry into the root but is essential to support arbuscule branching. In ram1-3, arbuscules consist only of the arbuscule trunk and in some cases, a few initial thick hyphal branches. ram1-3 is also insensitive to phosphate-mediated regulation of the symbiosis. Transcript analysis of ram1-3 and ectopic expression of RAM1 indicate that RAM1 regulates expression of EXO70I and Stunted Arbuscule, two genes whose loss of function impacts arbuscule branching. Furthermore, RAM1 regulates expression of a transcription factor Required for Arbuscule Development (RAD1). RAD1 is also required for arbuscular mycorrhizal symbiosis, and rad1 mutants show reduced colonization. RAM1 itself is induced in colonized root cortical cells, and expression of RAM1 and RAD1 is modulated by DELLAs. Thus, the data suggest that DELLAs regulate arbuscule development through modulation of RAM1 and RAD1 and that the precise transcriptional control essential to place proteins in the periarbuscular membrane is controlled, at least in part, by RAM1.

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“…5,6 The gene expression changes that underlie symbiotic development have been documented through detailed transcript profiling 7,8 and some transcriptional regulators have been identified, some of which are downstream components of the symbiosis signaling pathway. 4,[9][10][11] Development of AM symbiosis is also influenced by plant hormones and treatment of roots with gibberellic acid (GA) leads either to alterations in fungal entry into the root or abolishes arbuscule development. The precise outcome depends on the concentration of GA applied.…”

Section: Introductionmentioning

confidence: 99%

DELLA proteins regulate expression of a subset of AM symbiosis-induced genes inMedicago truncatula

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Park

et al. 2016

Plant Signaling & Behavior

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The majority of the vascular flowering plants form symbiotic associations with fungi from the phylum Glomeromycota through which both partners gain access to nutrients, either mineral nutrients in the case of the plant, or carbon, in the case of the fungus. 1 The association develops in the roots and requires substantial remodeling of the root cortical cells where branched fungal hyphae, called arbuscules, are housed in a new membrane-bound apoplastic compartment.2 Nutrient exchange between the symbionts occurs over this interface and its development and maintenance is critical for symbiosis. Previously, we showed that DELLA proteins, which are well known as repressors of gibberellic acid signaling, also regulate development of AM symbiosis and are necessary to enable arbuscule development.3 Furthermore, constitutive overexpression of a dominant DELLA protein (della1-D18) is sufficient to induce transcripts of several AM symbiosis-induced genes, even in the absence of the fungal symbiont. 4 Here we further extend this approach and identify AM symbiosis genes that respond transcriptionally to constitutive expression of a dominant DELLA protein and also genes that do respond to this treatment. Additionally, we demonstrate that DELLAs interact with REQUIRED FOR ARBUSCULE DEVELOPMENT 1 (RAD1) which further extends our knowledge of GRAS factor complexes that have the potential to regulate gene expression during AM symbiosis. Development of arbuscular mycorrhizal (AM) symbiosis involves signal exchange between the symbionts and a highly conserved plant symbiosis signaling pathway plays a central role in controlling fungal growth into the root and the development of the symbiotic interface in the cortical cells. 5,6 The gene expression changes that underlie symbiotic development have been documented through detailed transcript profiling 7,8 and some transcriptional regulators have been identified, some of which are downstream components of the symbiosis signaling pathway. 4,[9][10][11] Development of AM symbiosis is also influenced by plant hormones and treatment of roots with gibberellic acid (GA) leads either to alterations in fungal entry into the root or abolishes arbuscule development. The precise outcome depends on the concentration of GA applied.12 Genes encoding enzymes of GA biosynthesis and metabolism are differentially regulated during symbiosis 7,13-17 and associated with the colonized regions of the cortex.18 Furthermore, both bioactive and inactive GAs are present in mycorrhizal roots. All of these data suggest a role for GAs in regulating aspects of symbiotic development. 18,19 DELLA proteins are members of a specific sub-group of the GRAS family of transcriptional regulators that possess a unique domain, the DELLA domain, located toward the N-terminal end of the protein.20 DELLAs function as repressors of GA signaling and their mechanism of action has been elucidated through extensive studies in Arabidopsis. Briefly, in the presence of GA, the GA receptor (GID) interacts with the DELLAs through ...

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The Petunia GRAS Transcription Factor ATA/RAM1 Regulates Symbiotic Gene Expression and Fungal Morphogenesis in Arbuscular Mycorrhiza

Cited by 58 publications

References 70 publications

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

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

Hyphal branching during arbuscule development requires RAM1

DELLA proteins regulate expression of a subset of AM symbiosis-induced genes inMedicago truncatula

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