Nuclear-Localized and Deregulated Calcium- and Calmodulin-Dependent Protein Kinase Activates Rhizobial and Mycorrhizal Responses in <i>Lotus japonicus</i>

Takeda, Nobuo; Maekawa, Takaki; Hayashi, Makoto

doi:10.1105/tpc.111.091827

Cited by 88 publications

(74 citation statements)

References 66 publications

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“…Our model also opens up several questions, most important being: What is downstream of the G-protein cycle during nodulation? It is well established that the nuclear-localized CCaMK proteins are central to nodule development (Gleason et al, 2006;Tirichine et al, 2006;Takeda et al, 2012). How might the chain of events started at the level of plasma membrane-localized G-proteins be continued to the nuclear proteins?…”

Section: Mechanism Of G-protein Regulation Of Nodule Formationmentioning

confidence: 99%

“…One of the important downstream events involves changes in calcium spiking in and around the cell nucleus; these changes are sensed by a calcium/calmodulin-dependent protein kinase (CCaMK). Activation of CCaMK is central to the regulation of nodule development as its constitutive activation leads to spontaneous nodule formation (Tirichine et al, 2006;Hayashi et al, 2010;Liao et al, 2012;Takeda et al, 2012;Routray et al, 2013). Active CCaMK phosphorylates transcriptional activator CYCLOPS, which transactivates NODULE INCEPTION to initiate nodule development (Marsh et al, 2007;Singh et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Phosphorylation-Dependent Regulation of G-Protein Cycle during Nodule Formation in Soybean

Choudhury

Pandey

2015

Plant Cell

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ORCID IDs: 0000-0002-6738-3574 (S.R.C.); 0000-0002-5570-3120 (S.P.)Signaling pathways mediated by heterotrimeric G-protein complexes comprising Ga, Gb, and Gg subunits and their regulatory RGS (Regulator of G-protein Signaling) protein are conserved in all eukaryotes. We have shown that the specific Gb and Gg proteins of a soybean (Glycine max) heterotrimeric G-protein complex are involved in regulation of nodulation. We now demonstrate the role of Nod factor receptor 1 (NFR1)-mediated phosphorylation in regulation of the G-protein cycle during nodulation in soybean. We also show that during nodulation, the G-protein cycle is regulated by the activity of RGS proteins. Lower or higher expression of RGS proteins results in fewer or more nodules, respectively. NFR1 interacts with RGS proteins and phosphorylates them. Analysis of phosphorylated RGS protein identifies specific amino acids that, when phosphorylated, result in significantly higher GTPase accelerating activity. These data point to phosphorylation-based regulation of G-protein signaling during nodule development. We propose that active NFR1 receptors phosphorylate and activate RGS proteins, which help maintain the Ga proteins in their inactive, trimeric conformation, resulting in successful nodule development. Alternatively, RGS proteins might also have a direct role in regulating nodulation because overexpression of their phospho-mimic version leads to partial restoration of nodule formation in nod49 mutants.

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Section: Mechanism Of G-protein Regulation Of Nodule Formationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Phosphorylation-Dependent Regulation of G-Protein Cycle during Nodule Formation in Soybean

Choudhury

Pandey

2015

Plant Cell

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“…Development of AM symbiosis is controlled by the SSP; however, current data indicate that activation of the SSP pathway alone is not sufficient to induce the complete cortical transcriptional program associated with arbuscule formation (80) and that other pathways may be involved. To test the hypothesis that DELLA signaling for arbuscule formation might intersect with the SSP, the della1-Δ18 gene was expressed from the 35S promoter in a L. japonicus cyclops mutant, a M. truncatula ipd3 mutant, and in two additional symbiosis mutants, M. truncatula dmi3 and M. truncatula vapyrin, that are positioned upstream and downstream of cyclops/ipd3 in the SSP, respectively.…”

Section: Expression Of Della1-δ18 In the Vascular Tissue And Endodermismentioning

confidence: 60%

“…In dmi3 (ccamk) mutants the fungus fails to enter the cortex, but in cyclops mutants hyphal growth in the cortex occurs, suggesting partial activation of the cortical program. In L. japonicus, a gain-of-function ccamk mutant showed cellular changes in cortex which also suggest that CCAMK influences this phase of the symbiosis (80). An alternative interpretation is that arbuscule formation driven by della1-Δ18 has a less stringent requirement for CYCLOPS.…”

Section: Discussionmentioning

confidence: 99%

DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis

Floß

Lévy

Lévesque-Tremblay

et al. 2013

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

253

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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“…CCaMK is composed of a kinase domain and regulatory domains that include a calmodulinbinding domain and EF-hand motifs (Patil et al, 1995;Takezawa et al, 1996). The kinase activity is controlled by the regulatory domains; therefore, removal of these domains releases inhibition and stimulates the kinase activity, thus conferring gain-of-function properties (Takeda et al, 2012). The gain-of-function calcium-and calmodulin-dependent protein kinase (GOF-CCaMK) constitutively activates a part of the downstream symbiosis signaling pathway that induces arbuscular mycorrhiza-and RNS-induced gene expression and the formation of PPA-like structures without AM fungal infection.…”

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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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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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Nuclear-Localized and Deregulated Calcium- and Calmodulin-Dependent Protein Kinase Activates Rhizobial and Mycorrhizal Responses in Lotus japonicus

Cited by 88 publications

References 66 publications

Phosphorylation-Dependent Regulation of G-Protein Cycle during Nodule Formation in Soybean

Phosphorylation-Dependent Regulation of G-Protein Cycle during Nodule Formation in Soybean

DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis

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

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