Regulatory effects of nitric oxide on reproduction and melanin biosynthesis in onion pathogenic fungus Stemphylium eturmiunum

Zhao, Yuliang; Yuan, Wenwen; Sun, Mengni; Zhang, Xiuguo; Zheng, Wenhua

doi:10.1016/j.funbio.2021.01.010

Cited by 10 publications

(6 citation statements)

References 61 publications

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“…In previous studies, we and others observed that NO homeostasis regulates the balance between asexual and sexual reproduction (Maier et al, 2001;Marcos et al, 2016;Marcos et al, 2020;Zhao et al, 2021). Generally, higher levels of NO promote cleistothecia formation whereas, at the same time, it represses conidiation.…”

Section: Growth On Arginine Reduces Conidiationmentioning

confidence: 78%

Evidence for an arginine‐dependent route for the synthesis of NO in the model filamentous fungus Aspergillus nidulans

Franco-Cano

Marcos

Strauss

et al. 2021

Environmental Microbiology

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Nitric oxide (NO) is a signalling molecule in eukaryotic and prokaryotic organisms. NO levels transiently boost upon induction of conidiation in Aspergillus nidulans. Only one pathway for NO synthesis involving nitrate reductase has been reported in filamentous fungi so far, but this does not satisfy all the NO produced in fungal cells. Here we provide evidence for at least one additional biosynthetic pathway in A. nidulans involving L-arginine or an intermediate metabolite as a substrate. Under certain growth conditions, the addition of L-arginine to liquid media elicited a burst of NO that was not dependent on any of the urea cycle genes. The NO levels were controlled by the metabolically available arginine, which was regulated by mobilization from the vacuoles and during development. In vitro assays with protein extracts and amino acid profiling strongly suggested the existence of an arginine-dependent NO pathway analogous to the mammalian NO synthase. Addition of polyamines induced NO synthesis, and mutations in the polyamine synthesis genes puA and spdA reduced the production of NO. In conclusion, here we report an additional pathway for the synthesis of NO in A. nidulans using urea cycle intermediates.

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Section: Growth On Arginine Reduces Conidiationmentioning

confidence: 78%

Evidence for an arginine‐dependent route for the synthesis of NO in the model filamentous fungus Aspergillus nidulans

Franco-Cano

Marcos

Strauss

et al. 2021

Environmental Microbiology

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“…Furthermore, based on our previous transcriptional analysis of S. bambusicola S8 under red light (Ma et al 2019a ), we analyzed the expression levels of genes related to sporulation, including sexual differentiation process protein ( ISP7 ), cleistothecium development ( CSN3 ), stage v sporulation protein k ( SSPK ), 30 kDa heat shock protein ( HSP30 ), and transcriptional factor BrlA and WetA . These genes have been reported to be responsive to external NO application and be also related to fungal conidiation (Boylan et al 1987 ; Zhao et al 2021b ). In our study, their expressions were significantly down-regulated by red light, about 4.5-, 8.8-, 3.7-, 2.8-, 2.1-, 2.5-fold relative to the control, respectively.…”

Section: Resultsmentioning

confidence: 99%

“…The primer of genes related to the sporulation (Ma et al 2019a ; Zhao et al 2021b ), genes for HA biosynthesis and internal reference gene (18S ribosomal RNA) are listed in Additional file 1 : Table S1. The real-time quantitative PCR (RT-qPCR) was measured in the CFX96-C1000 Touch Real-Time PCR Detection System (Bio-Rad, Hercules, CA, USA) for gene transcription analysis.…”

Section: Methodsmentioning

confidence: 99%

Nitric oxide mediates red light-induced perylenequinone production in Shiraia mycelium culture

Wang,

Li,

Shen

et al. 2024

Bioresour. Bioprocess.

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Perylenequinones (PQs) from bambusicolous Shiraia fungi serve as excellent photosensitizers for photodynamic therapy. However, the lower yield of PQ production in mycelium cultures is an important bottleneck for their clinical application. Light has long been recognized as a pivotal regulatory signal for fungal secondary metabolite biosynthesis. In this study, we explored the role of nitric oxide (NO) in the growth and PQ biosynthesis in mycelium cultures of Shiraia sp. S9 exposed to red light. The continuous irradiation with red light (627 nm, 200 lx) suppressed fungal conidiation, promoted hyphal branching, and elicited a notable increase in PQ accumulation. Red light exposure induced NO generation, peaking to 81.7 μmol/g FW on day 8 of the culture, with the involvement of nitric oxide synthase (NOS)- or nitrate reductase (NR)-dependent pathways. The application of a NO donor sodium nitroprusside (SNP) restored conidiation of Shiraia sp. S9 under red light and stimulated PQ production, which was mitigated upon the introduction of NO scavenger carboxy-PTIO or soluble guanylate cyclase inhibitor NS-2028. These results showed that red light-induced NO, as a signaling molecule, was involved in the regulation of growth and PQ production in Shiraia sp. S9 through the NO-cGMP-PKG signaling pathway. While mycelial H2O2 content exhibited no significant alternations, a transient increase of intracellular Ca2+ and extracellular ATP (eATP) content was detected upon exposure to red light. The generation of NO was found to be interdependent on cytosolic Ca2+ and eATP concentration. These signal molecules cooperated synergistically to enhance membrane permeability and elevate the transcript levels of PQ biosynthetic genes in Shiraia sp. S9. Notably, the combined treatment of red light with 5 μM SNP yielded a synergistic effect, resulting in a substantially higher level of hypocrellin A (HA, 254 mg/L), about 3.0-fold over the dark control. Our findings provide valuable insights into the regulation of NO on fungal secondary metabolite biosynthesis and present a promising strategy involving the combined elicitation with SNP for enhanced production of photoactive PQs and other valuable secondary metabolites in fungi. Graphical Abstract

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“…In Stemphylium eturmiunum , enhanced melanin biosynthesis correlates with an increased formation of propagules [ 48 ]. Conidiogenesis in black, white and mixed subpopulations of Cochliobolus sativus was positively correlated with the melanin content of mycelium [ 49 ].…”

Section: Discussionmentioning

confidence: 99%

A Melanin-Deficient Isolate of Venturia inaequalis Reveals Various Roles of Melanin in Pathogen Life Cycle and Fitness

Steiner

Oerke

2022

JoF

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Venturia inaequalis is the ascomycetous pathogen causing apple scabs and forms dark-pigmented spores and partially melanised infection structures. Although melanin is considered to be essential for the infection of host tissue, a spontaneously occurring melanin-deficient mutant was isolated from an abaxial side of an apple leaf and can be cultivated in vitro as well as in vivo. The morphology and development of the melanin-deficient-isolate SW01 on leaves of susceptible apple plants were compared to that of the corresponding wild-type isolate HS1. White conidia of SW01 were often wrinkled when dry and significantly increased their volume in suspension. Germination and formation of germtubes and appressoria were not impaired; however, the lack of melanisation of the appressorial ring structure at the interface with the plant cuticle significantly reduced the infection success of SW01. The colonisation of leaf tissue by non-melanised subcuticular hyphae was not affected until the initiation of conidiogenesis. Non-melanised conidiophores penetrated the plant cuticle from inside less successfully than the wild type, and the release of white conidia from less solid conidiophores above the cuticle was less frequent. Melanin in the outer cell wall of V. inaequalis was not required for the survival of conidia under ambient temperature or at −20 °C storage conditions, however, promoted the tolerance of the pathogen to copper and synthetic fungicides affecting the stability and function of the fungal cell wall, plasma membrane, respiration (QoIs) and enzyme secretion, but had no effect on the sensitivity to sulphur and SDHIs. The roles of melanin in different steps of the V. inaequalis life cycle and the epidemiology of apple scabs are discussed.

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Regulatory effects of nitric oxide on reproduction and melanin biosynthesis in onion pathogenic fungus Stemphylium eturmiunum

Cited by 10 publications

References 61 publications

Evidence for an arginine‐dependent route for the synthesis of NO in the model filamentous fungus Aspergillus nidulans

Evidence for an arginine‐dependent route for the synthesis of NO in the model filamentous fungus Aspergillus nidulans

Nitric oxide mediates red light-induced perylenequinone production in Shiraia mycelium culture

A Melanin-Deficient Isolate of Venturia inaequalis Reveals Various Roles of Melanin in Pathogen Life Cycle and Fitness

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