Nitric oxide as a developmental and metabolic signal in filamentous fungi

Zhao, Yuliang; Lim, Jieyin; Xu, Jing; Yu, Jae‐Hyuk; Zheng, Wenhua

doi:10.1111/mmi.14465

Cited by 48 publications

(40 citation statements)

References 87 publications

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“…Several studies have reported that sporulation in lamentous fungi is promoted by application of external NO but inhibited by sGC inhibitor L-NAME or ODQ. However, sporulation can be restored by exogenous cGMP (Zhao et al 2020). In our study, NO promoted formation of conidia and pseudothecia, and melanin production can also be compromised by sGC speci c inhibitor NS-2080 even in the presence of SNP.…”

Section: Discussionsupporting

confidence: 45%

“…Cellular NO levels also affect sexual development in lamentous fungi (reviewed by Zhao et al 2020). In Aspergillus nidulans, the increase in cellular NO levels by disrupting the genes encoding avohemoglobin or supplementing NO-releasing compound promotes the formation of cleistothecia (Baidya et a., 2011).…”

Section: Discussionmentioning

confidence: 99%

“…The well-known signaling pathways in fungi include the protein kinase A/cyclic AMP (cAMP), protein kinase G/cyclic GMP (cGMP), protein kinase C (PKC)/mitogenactivated protein kinase (MAPK), lipid signaling cascades, and the calcium-calcineurin signaling pathway (Kozubowski et al 2009). PKG/cGMP pathway, which seems to exist in lamentous fungi, is activated by free radical molecule NO (Zhao et al 2020). The NO, highly diffusible within the cell or through cell membrane (Lancaster 1997), can work as a transient, local, intra-or intercellular signaling molecule in miscellaneous biological systems including fungi (Culotta and Koshland 1992).…”

Section: Introductionmentioning

confidence: 99%

“…The NO, highly diffusible within the cell or through cell membrane (Lancaster 1997), can work as a transient, local, intra-or intercellular signaling molecule in miscellaneous biological systems including fungi (Culotta and Koshland 1992). In fungi, NO signaling is involved in conidiation, formation of sexual fruiting bodies, and regulation of secondary metabolism (Zhao et al 2020). Established evidences have shown that NO can function as the activator of sGC able to bind selectively with the hemoprotein in sGC even in the presence of oxygen (Boon and Marletta 2005).…”

Section: Introductionmentioning

confidence: 99%

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Regulatory Effects of Nitric Oxide on Reproduction and Melanin Biosynthesis in Onion Pathogenic Fungus Stemphylium Eturmiunum

Zhao

Yuan

Sun

et al. 2020

Preprint

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The formation of propagules (conidia and ascospores) is the critical stage for the transmission of the pathogenic fungus Stemphylium eturmiunum. However, how the development of these propagules is regulated remains to be fully understood. Here, we show that nitric oxide (NO) is necessary for the formation of conidia and pseudothecia in S. eturmiunum. Application of NO scavenger carboxy-CPTIO (cPTIO) or soluble guanylate cyclase (sGC) inhibitor NS2028 abolishes the formation of conidia and pseudothecia. In the culture of S. eturmiunum, supplement of NO-releasing compound sodium nitroprusside (SNP) results in an increased formation of conidia at 0.2 mmol/L, and pseudothecia at 2 mmol/L. SNP supplement also triggered increased biosynthesis of melanin, which can be inhibited partially upon the addition of either arbutin or tricyclazole, the specific inhibitors for 3,4-dihydroxyphenylalanine (DOPA) and dihydroxynaphthalene (DHN) synthetic pathway, respectively. Intriguingly, enhanced melanin biosynthesis triggered an increased formation of propagules; while its inhibition impaired their formation. The SNP-induced increment in the formation of propagules can be also compromised upon supplement of cPTIO or NS-2028. RT-PCR analysis showed that SNP at 0.2 mmol/L promoted transcription of the genes encoding the conidiation co-regulators brlA, abA, and wetA, and inhibited at 2 mmol/L. In contrast, application of SNP at 2 mmol/L increased transcription of the genes encoding mat1, and mat2, the genes related to sexual reproduction, and the transcription of two DNH melanin synthetic genes pks1 and pks2, and the key gene tyr for DOPA melanin biosynthesis. However, the increased transcription of these genes is down-regulated or blocked upon supplement of cPTIO or NS-2028. Thus, NO regulates asexual and sexual development, as well as melanin synthesis in S. eturmiunum possibly through NO-sGC-GMP signaling pathway.

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Section: Discussionsupporting

confidence: 45%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Regulatory Effects of Nitric Oxide on Reproduction and Melanin Biosynthesis in Onion Pathogenic Fungus Stemphylium Eturmiunum

Zhao

Yuan

Sun

et al. 2020

Preprint

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“…In fungi, NO is synthesized through a reductive denitrification pathway from nitrite, and through an oxidative pathway from L-arginine, although the detailed biochemical mechanisms have not yet been fully elucidated (11)(12)(13). Compared to mammals, plants, and bacteria, the role of NO in fungal biology is understudied.…”

Section: Significancementioning

confidence: 99%

HGT in the human and skin commensal Malassezia : A bacterially derived flavohemoglobin is required for NO resistance and host interaction

Ianiri

Coelho

Ruchti

et al. 2020

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

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The skin of humans and animals is colonized by commensal and pathogenic fungi and bacteria that share this ecological niche and have established microbial interactions.Malasseziaare the most abundant fungal skin inhabitant of warm-blooded animals and have been implicated in skin diseases and systemic disorders, including Crohn’s disease and pancreatic cancer. Flavohemoglobin is a key enzyme involved in microbial nitrosative stress resistance and nitric oxide degradation. Comparative genomics and phylogenetic analyses within theMalasseziagenus revealed that flavohemoglobin-encoding genes were acquired through independent horizontal gene transfer events from different donor bacteria that are part of the mammalian microbiome. Through targeted gene deletion and functional complementation inMalassezia sympodialis, we demonstrated that bacterially derived flavohemoglobins are cytoplasmic proteins required for nitric oxide detoxification and nitrosative stress resistance under aerobic conditions. RNA-sequencing analysis revealed that endogenous accumulation of nitric oxide resulted in up-regulation of genes involved in stress response and down-regulation of the MalaS7 allergen-encoding genes. Solution of the high-resolution X-ray crystal structure ofMalasseziaflavohemoglobin revealed features conserved with both bacterial and fungal flavohemoglobins. In vivo pathogenesis is independent ofMalasseziaflavohemoglobin. Lastly, we identified an additional 30 genus- and species-specific horizontal gene transfer candidates that might have contributed to the evolution of this genus as the most common inhabitants of animal skin.

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