Correlation of nitric oxide produced by an inducible nitric oxide synthase-like protein with enhanced expression of the phenylpropanoid pathway in Inonotus obliquus cocultured with Phellinus morii

Zhao, Yuliang; Xi, Qi; Xu, Qian; He, Meihong; Ding, Jingjin; Dai, Yu-Cheng; Keller, Nancy P.; Zheng, Wenhua

doi:10.1007/s00253-014-6367-2

Cited by 31 publications

(30 citation statements)

References 45 publications

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“…A rapid nitrosative burst following fungal recognition drives NO accumulation, which activates the transcription of genes in phenylpropanoid metabolism required for styrylpyrone polyphenol biosynthesis4 followed by S-nitrosylation of PAL, 4CL and SPS12. Our data further confirm that these key enzymes in the biosynthesis of these natural products are S-nitrosylated and this modification reduces their activity, decreasing production of styrylpyrone polyphenols.…”

Section: Discussionsupporting

confidence: 73%

“…The phenylpropanoid pathway is integral to styrylpyrone biosynthesis and PAL and 4CL are key enzymes for the production of phenylpropanoid related metabolites4. The regulation of the phenylpropanoid synthesis is principally thought to occur at a transcriptional level25.…”

Section: Discussionmentioning

confidence: 99%

“…A nitrosative burst, leading to the production of the redox cue, nitric oxide (NO), is thought to be integral to this process4. Further, an elevated level of NO-driven S-nitrosylation, the addition of a NO moiety to a reactive protein cysteine (Cys) thiol to form a S-nitrosothiol (SNO)56 was also detected7.…”

mentioning

confidence: 99%

“…A recent study suggests that the coculture of I. obliquus and Phellinus morii promotes increased phenylpropanoid-related gene expression followed by a transient increase in the production of styrylpyrone polyphenols4. Further, coculture of these two fungi also triggers NO burst and the subsequent S-nitrosylation of the key enzymes in styrylpyrone biosynthesis12.…”

mentioning

confidence: 99%

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Regulation of Anticancer Styrylpyrone Biosynthesis in the Medicinal Mushroom Inonotus obliquus Requires Thioredoxin Mediated Transnitrosylation of S-nitrosoglutathione Reductase

Zhao

Ding

et al. 2016

Sci Rep

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The medicinal macrofungus Inonotus obliquus widely utilized as folk medicine in Russia and Baltic countries is a source of phenylpropanoid-derived styrylpyrone polyphenols that can inhibit tumor proliferation. Insights into the regulatory machinery that controls I. obliquus styrylpyrone polyphenol biosynthesis will enable strategies to increase the production of these molecules. Here we show that Thioredoxin (Trx) mediated transnitrosylation of S-nitrosoglutathione reductase (GSNOR) underpins the regulation of styrylpyrone production, driven by nitric oxide (NO) synthesis triggered by P. morii coculture. NO accumulation results in the S-nitrosylation of PAL and 4CL required for the synthesis of precursor phenylpropanoids and styrylpyrone synthase (SPS), integral to the production of styrylpyrone, inhibiting their activities. These enzymes are targeted for denitrosylation by Trx proteins, which restore their activity. Further, this Trx S-nitrosothiol (SNO) reductase activity was potentiated following S-nitrosylation of Trx proteins at a non-catalytic cysteine (Cys) residue. Intriguingly, this process was counterbalanced by Trx denitrosylation, mediated by Trx-dependent transnitrosylation of GSNOR. Thus, unprecedented interplay between Trx and GSNOR oxidoreductases regulates the biosynthesis of styrylpyrone polyphenols in I. obliquus.

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Section: Discussionsupporting

confidence: 73%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Regulation of Anticancer Styrylpyrone Biosynthesis in the Medicinal Mushroom Inonotus obliquus Requires Thioredoxin Mediated Transnitrosylation of S-nitrosoglutathione Reductase

Zhao

Ding

et al. 2016

Sci Rep

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“…Alternatively, increases in ROS levels may function as a defence signalling response similar to that in plants, for example, triggering biosynthesis of pigment (94,96). Increases in another potential signalling compound, nitric oxide (NO), have also been detected during interactions between Phellinus morii and Inonotus obliquus, triggering the production of antifungal phenylpropanoid metabolites (97).…”

Section: Accumulation Of Rosmentioning

confidence: 99%

Fungal Ecology: Principles and Mechanisms of Colonization and Competition by Saprotrophic Fungi

2016

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Decomposer fungi continually deplete the organic resources they inhabit, so successful colonization of new resources is a crucial part of their ecology. Colonization success can be split into (i) the ability to arrive at, gain entry into, and establish within a resource and (ii) the ability to persist within the resource until reproduction and dissemination. Fungi vary in their life history strategies, the three main drivers of which are stress (S-selected), disturbance (ruderal, or R-selected), and incidence of competitors (C-selected); however, fungi often have combinations of characteristics from different strategies. Arrival at a new resource may occur as spores or mycelium, with successful entry and establishment (primary resource capture) within the resource largely dependent on the enzymatic ability of the fungus. The communities that develop in a newly available resource depend on environmental conditions and, in particular, the levels of abiotic stress present (e.g., high temperature, low water availability). Community change occurs when these initial colonizers are replaced by species that are either more combative (secondary resource capture) or better able to tolerate conditions within the resource, either through changing abiotic conditions or due to modification of the resource by the initial colonizers. Competition for territory may involve highly specialized species-specific interactions such as mycoparasitism or may be more general; in both cases combat involves changes in morphology, metabolism, and reactive oxygen species production, and outcomes of these interactions can be altered under different environmental conditions. In summary, community development is not a simple ordered sequence, but a complex ever-changing mosaic.

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Reversible S-nitrosylation limits over synthesis of fungal styrylpyrone upon nitric oxide burst

Zhao

et al. 2016

Appl Microbiol Biotechnol

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Nitric oxide (NO) is known to be involved in modulating production of styrylpyrone polyphenols in the basidiomycete Inonotus obliquus. However, it remains unknown how NO orchestrates fungal styrylpyrone biosynthesis. Here, we show that a transient NO burst correlated with an enhanced expression of phenylalanine ammonia lyase (PAL), 4-coumarate CoA ligase (4CL), and styrylpyrone synthase (SPS), the key enzymes involved in styrylpyrone biosynthesis, and subsequently an increased production of styrylpyrone polyphenols. In parallel, the NO burst also resulted in S-nitrosylation of PAL, 4CL, and SPS, which compromised their enzymatic activities mediating a post-translational feedback mechanism that keeps NO-dependent transcriptional activation in check. Moreover, dysfunction of thioredoxin reductase (TrxR) further increased the formation of S-nitrosylated proteins, implicating the significance of the Trx system in maintaining a low level of protein-nitrosothiols. Three thioredoxin-like proteins (TrxLs) from I. obliquus show in vitro denitrosylation potential toward S-nitrosylated proteins via trans-denitrosylation or mixed disulfide intermediates. Thus, S-nitrosylation triggered by the NO burst limits over production of fungal styrylpyrone polyphenols, and denitrosylation by TrxLs that act in concert with TrxR play a key role in maintaining redox balance and orchestrating catalytic activities of the enzymes engaged in styrylpyrone synthetic metabolism.

show abstract

Correlation of nitric oxide produced by an inducible nitric oxide synthase-like protein with enhanced expression of the phenylpropanoid pathway in Inonotus obliquus cocultured with Phellinus morii

Cited by 31 publications

References 45 publications

Regulation of Anticancer Styrylpyrone Biosynthesis in the Medicinal Mushroom Inonotus obliquus Requires Thioredoxin Mediated Transnitrosylation of S-nitrosoglutathione Reductase

Regulation of Anticancer Styrylpyrone Biosynthesis in the Medicinal Mushroom Inonotus obliquus Requires Thioredoxin Mediated Transnitrosylation of S-nitrosoglutathione Reductase

Fungal Ecology: Principles and Mechanisms of Colonization and Competition by Saprotrophic Fungi

Reversible S-nitrosylation limits over synthesis of fungal styrylpyrone upon nitric oxide burst

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