Plant Genes Related to Gibberellin Biosynthesis and Signaling Are Differentially Regulated during the Early Stages of AM Fungal Interactions

Ortu, G.; Balestrini, Raffaella; Pereira, Patrícia A.; Becker, Jörg; Küster, H.; Bonfante, Paola

doi:10.1093/mp/sss027

Cited by 38 publications

(35 citation statements)

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“…1, B and D). The up-regulation of GA biosynthesis and metabolism genes during arbuscular mycorrhiza also was reported in AM plants (Gomez et al, 2009;Guether et al, 2009;Ortu et al, 2012). Histochemical analyses of both arbuscular mycorrhiza-induced GA 20-oxidases (GA20ox1 and GA20ox2), suggested to be key enzymes controlling GA amounts (Middleton et al, 2012), by using GUS fusions revealed that the up-regulation of GA biosynthesis occurs around AM hyphae in the host root during AM colonization (Fig.…”

Section: Discussion Am Fungal Infection Induces the Biosynthesis And supporting

confidence: 57%

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Gibberellins Interfere with Symbiosis Signaling and Gene Expression and Alter Colonization by Arbuscular Mycorrhizal Fungi in Lotus japonicus

et al. 2014

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Arbuscular mycorrhiza is a mutualistic plant-fungus interaction that confers great advantages for plant growth. Arbuscular mycorrhizal (AM) fungi enter the host root and form symbiotic structures that facilitate nutrient supplies between the symbionts. The gibberellins (GAs) are phytohormones known to inhibit AM fungal infection. However, our transcriptome analysis and phytohormone quantification revealed GA accumulation in the roots of Lotus japonicus infected with AM fungi, suggesting that de novo GA synthesis plays a role in arbuscular mycorrhiza development. We found pleiotropic effects of GAs on the AM fungal infection. In particular, the morphology of AM fungal colonization was drastically altered by the status of GA signaling in the host root. Exogenous GA treatment inhibited AM hyphal entry into the host root and suppressed the expression of Reduced Arbuscular Mycorrhization1 (RAM1) and RAM2 homologs that function in hyphal entry and arbuscule formation. On the other hand, inhibition of GA biosynthesis or suppression of GA signaling also affected arbuscular mycorrhiza development in the host root. Low-GA conditions suppressed arbuscular mycorrhiza-induced subtilisin-like serine protease1 (SbtM1) expression that is required for AM fungal colonization and reduced hyphal branching in the host root. The reduced hyphal branching and SbtM1 expression caused by the inhibition of GA biosynthesis were recovered by GA treatment, supporting the theory that insufficient GA signaling causes the inhibitory effects on arbuscular mycorrhiza development. Most studies have focused on the negative role of GA signaling, whereas our study demonstrates that GA signaling also positively interacts with symbiotic responses and promotes AM colonization of the host root.

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Section: Discussion Am Fungal Infection Induces the Biosynthesis And supporting

confidence: 57%

“…It has been suggested that GA signaling contributes to arbuscular mycorrhiza and RNS despite its negative effects on symbioses (El Ghachtouli et al, 1996;Ortu et al, 2012;Song et al, 2012). Here, we report the upregulation of GA biosynthesis and the accumulation of GAs in the roots of L. japonicus during arbuscular mycorrhiza development.…”

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confidence: 99%

Gibberellins Interfere with Symbiosis Signaling and Gene Expression and Alter Colonization by Arbuscular Mycorrhizal Fungi in Lotus japonicus

et al. 2014

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“…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][14][15][16][17] and associated with the colonized regions of the cortex. 18 Furthermore, both bioactive and inactive GAs are present in mycorrhizal roots.…”

Section: Introductionmentioning

confidence: 99%

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

Floß

Lévesque-Tremblay

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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“…Transcriptome analyses reveal substantial alterations in the expression of genes encoding enzymes of gibberellic acid (GA) biosynthesis, degradation, and signaling during AM symbiosis (28,(35)(36)(37)(38)(39). Consistent with these alterations, GA levels increase significantly in mycorrhizal roots (40).…”

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confidence: 98%

DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis

Floß

Lévy

Lévesque-Tremblay

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

251

267

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Most flowering plants are able to form endosymbioses with arbuscular mycorrhizal fungi. In this mutualistic association, the fungus colonizes the root cortex and establishes elaborately branched hyphae, called arbuscules, within the cortical cells. Arbuscule development requires the cellular reorganization of both symbionts, and the resulting symbiotic interface functions in nutrient exchange. A plant symbiosis signaling pathway controls the development of the symbiosis. Several components of the pathway have been identified, but transcriptional regulators that control downstream pathways for arbuscule formation are still unknown. Here we show that DELLA proteins, which are repressors of gibberellic acid (GA) signaling and function at the nexus of several signaling pathways, are required for arbuscule formation. Arbuscule formation is severely impaired in a Medicago truncatula Mtdella1/Mtdella2 double mutant; GA treatment of wild-type roots phenocopies the della double mutant, and a dominant DELLA protein (della1-Δ18) enables arbuscule formation in the presence of GA. Ectopic expression of della1-Δ18 suggests that DELLA activity in the vascular tissue and endodermis is sufficient to enable arbuscule formation in the inner cortical cells. In addition, expression of della1-Δ18 restores arbuscule formation in the symbiosis signaling pathway mutant cyclops/ipd3, indicating an intersection between DELLA and symbiosis signaling for arbuscule formation. GA signaling also influences arbuscule formation in monocots, and a Green Revolution wheat variety carrying dominant DELLA alleles shows enhanced colonization but a limited growth response to arbuscular mycorrhizal symbiosis.endosymbiosis | phytohormone | biotrophic | cyclops | Lotus japonicus

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Plant Genes Related to Gibberellin Biosynthesis and Signaling Are Differentially Regulated during the Early Stages of AM Fungal Interactions

Cited by 38 publications

References 9 publications

Gibberellins Interfere with Symbiosis Signaling and Gene Expression and Alter Colonization by Arbuscular Mycorrhizal Fungi in Lotus japonicus

Gibberellins Interfere with Symbiosis Signaling and Gene Expression and Alter Colonization by Arbuscular Mycorrhizal Fungi in Lotus japonicus

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

DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis

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