Glutamate synthase MoGlt1‐mediated glutamate homeostasis is important for autophagy, virulence and conidiation in the rice blast fungus

Zhou, Wei; Shi, Wei; Xu, Xiaowen; Li, Zhigang; Yin, Changfa; Peng, Junbo; Pan, Song; Chen, Xiao‐Lin; Zhao, Wensheng; Zhang, Yan; Yang, Jun; Peng, You-Liang

doi:10.1111/mpp.12541

Cited by 34 publications

(29 citation statements)

References 65 publications

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“…The Δ VdAtf1 strain exhibited reduced efficiency in using NH 4 + and therefore may cause inadequate ammonium conversion to glutamate. Under such conditions, the synthesis of amino acids becomes disordered and cellular stability suffers, ultimately causing growth inhibition (Sakamoto et al , 2009; Marroquin‐Guzman & Wilson, 2015; Zhou et al , 2018). In A. oryzae , the concentration of glutamate was significantly lower in the AtfA mutant compared to the wide type, suggesting AtfA controls amino acid accumulation that is necessary for a high germination ratio (Sakamoto et al , 2009), in accordance with our results on the analyses of the Δ VdAtf1 strain.…”

Section: Discussionmentioning

confidence: 99%

The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae

Tang

Klosterman

et al. 2020

New Phytologist

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The fungus Verticillium dahliae causes vascular wilt disease on hundreds of plant species. Homologs of the bZIP transcription factor Atf1 are required for virulence in most pathogenic fungi, but the molecular basis for their involvement is largely unknown.We performed targeted gene deletion, expression analysis, biochemistry and pathogenicity assays to demonstrate that VdAtf1 governs pathogenesis via the regulation of nitrosative resistance and nitrogen metabolism in V. dahliae.VdAtf1 controls pathogenesis via the regulation of nitric oxide (NO) resistance and inorganic nitrogen metabolism rather than oxidative resistance and is important for penetration peg formation in V. dahliae. VdAtf1 affects ammonium and nitrate assimilation in response to various nitrogen sources. VdAtf1 may be involved in regulating the expression of VdNut1. VdAtf1 responds to NO stress by strengthening the fungal cell wall, and by causing over-accumulation of methylglyoxal and glycerol, which in turn impacts NO detoxification. We also verified that the VdAtf1 ortholog in Fusarium graminearum mediates nitrogen metabolism, suggesting conservation of this function in related plant pathogenic fungi.Our findings revealed new functions of VdAtf1 in pathogenesis, response to nitrosative stress and nitrogen metabolism in V. dahliae. The results provide novel insights into the regulatory mechanisms of the transcription factor VdAtf1 in virulence.

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Section: Discussionmentioning

confidence: 99%

The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae

Tang

Klosterman

et al. 2020

New Phytologist

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“…Alterations in cellular PAs due to inactivation of PA biosynthetic genes ( spds , odc ) in A. nidulans were reported in earlier studies ( Jin et al, 2002 ; Khatri and Rajam, 2007 ), but the current data show that alterations in Spd levels in A. flavus goes beyond the PA biosynthetic pathway and affects biosynthesis of AAs. Several of the AAs (such as Glu, Ser, Thr) that were decreased in the Δspds mutant ( Table 1 ) are reported to be critical in fungal pathogenesis ( Olivieri et al, 2002 ; de Sain and Rep, 2015 ; Muszewska et al, 2017 ; Zhou et al, 2017 ). Whether the reduction in pathogenicity in the Δspds mutant during maize seed infection is due to the decrease in Spd or possible alteration in relative AA content or both, will require further investigation.…”

Section: Discussionmentioning

confidence: 99%

The Aspergillus flavus Spermidine Synthase (spds) Gene, Is Required for Normal Development, Aflatoxin Production, and Pathogenesis During Infection of Maize Kernels

et al. 2018

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Aspergillus flavus is a soil-borne saprophyte and an opportunistic pathogen of both humans and plants. This fungus not only causes disease in important food and feed crops such as maize, peanut, cottonseed, and tree nuts but also produces the toxic and carcinogenic secondary metabolites (SMs) known as aflatoxins. Polyamines (PAs) are ubiquitous polycations that influence normal growth, development, and stress responses in living organisms and have been shown to play a significant role in fungal pathogenesis. Biosynthesis of spermidine (Spd) is critical for cell growth as it is required for hypusination-mediated activation of eukaryotic translation initiation factor 5A (eIF5A), and other biochemical functions. The tri-amine Spd is synthesized from the diamine putrescine (Put) by the enzyme spermidine synthase (Spds). Inactivation of spds resulted in a total loss of growth and sporulation in vitro which could be partially restored by addition of exogenous Spd. Complementation of the Δspds mutant with a wild type (WT) A. flavus spds gene restored the WT phenotype. In WT A. flavus, exogenous supply of Spd (in vitro) significantly increased the production of sclerotia and SMs. Infection of maize kernels with the Δspds mutant resulted in a significant reduction in fungal growth, sporulation, and aflatoxin production compared to controls. Quantitative PCR of Δspds mutant infected seeds showed down-regulation of aflatoxin biosynthetic genes in the mutant compared to WT A. flavus infected seeds. Expression analyses of PA metabolism/transport genes during A. flavus-maize interaction showed significant increase in the expression of arginine decarboxylase (Adc) and S-adenosylmethionine decarboxylase (Samdc) genes in the maize host and PA uptake transporters in the fungus. The results presented here demonstrate that Spd biosynthesis is critical for normal development and pathogenesis of A. flavus and pre-treatment of a Δspds mutant with Spd or Spd uptake from the host plant, are insufficient to restore WT levels of pathogenesis and aflatoxin production during seed infection. The data presented here suggest that future studies targeting spermidine biosynthesis in A. flavus, using RNA interference-based host-induced gene silencing approaches, may be an effective strategy to reduce aflatoxin contamination in maize and possibly in other susceptible crops.

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“…To observe nuclei of barley cells, samples were stained with 1 μg ml −1 4′,6‐diamidino‐2‐phenylindole (DAPI) as described previously (Xu and Hamer, ). Differential interference contrast and epi‐fluorescence images were performed with an epi‐fluorescence microscope (Nikon, https://www.nikon.com; Zhou et al ., ). Filter sets used were as follows: mCherry (excitation 510–560 nm; emission 575–590 nm) and DAPI (excitation 330–380 nm; emission 400–420 nm).…”

Section: Methodsmentioning

confidence: 97%

A positive‐charged patch and stabilized hydrophobic core are essential for avirulence function of AvrPib in the rice blast fungus

Zhang

Zhao

et al. 2018

The Plant Journal

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Fungal avirulence effectors, a key weapon utilized by pathogens to promote their infection, are recognized by immune receptors to boost host R gene-mediated resistance. Many avirulence effectors share sparse sequence homology to proteins with known functions, and their molecular and biochemical functions together with the evolutionary relationship among different members remain largely unknown. Here, the crystal structure of AvrPib, an avirulence effector from Magnaporthe oryzae, was determined and showed a high degree of similarity to the M. oryzae Avrs and ToxB (MAX) effectors. Compared with other MAX effectors, AvrPib has a distinct positive-charge patch formed by five positive-charged residues (K29, K30, R50, K52 and K70) on the surface. These five key residues were essential to avirulence function of AvrPib and affected its nuclear localization into host cells. Moreover, residues V39 and V58, which locate in the hydrophobic core of the structure, cause loss of function of AvrPib by single-point mutation in natural isolates. In comparison with the wild-type AvrPib, the V39A or V58A mutations resulted in a partial or entire loss of secondary structure elements. Taken together, our results suggest that differences in the surface charge distribution of avirulence proteins could be one of the major bases for the variation in effector-receptor specificity, and that destabilization of the hydrophobic core is one of the major mechanisms employed by AvrPib for the fungus to evade recognition by resistance factors in the host cell.

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Glutamate synthase MoGlt1‐mediated glutamate homeostasis is important for autophagy, virulence and conidiation in the rice blast fungus

Cited by 34 publications

References 65 publications

The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae

The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae

The Aspergillus flavus Spermidine Synthase (spds) Gene, Is Required for Normal Development, Aflatoxin Production, and Pathogenesis During Infection of Maize Kernels

A positive‐charged patch and stabilized hydrophobic core are essential for avirulence function of AvrPib in the rice blast fungus

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