Dataset Information

Update on Nox function, site of action and regulation in Botrytis cinerea.

ABSTRACT:

Background

The production of reactive oxygen species (ROS) and a balanced redox homeostasis are essential parameters, which control the infection process of the plant pathogen Botrytis cinerea. The necrotrophic fungus is able to cope with the plants' oxidative burst and even produces its own ROS to overcome the plants' defense barrier. Major enzyme complexes, which are responsible for the production of superoxide, are NADPH oxidase (Nox) complexes. They play a central role in various growth, differentiation and pathogenic processes. However, information about their regulation and the integration in the complex signaling network of filamentous fungi is still scarce.

Results

In this work, we give an update on Nox structure, function, site of action and regulation. We show that functionality of the catalytic Nox-subunits seems to be independent from their transcriptional regulation and that the membrane orientation of BcNoxA would allow electron transport inside the ER. Following previous studies, which provided evidence for distinct functions of the NoxA complex inside the ER, we highlight in this work that the N-terminus of BcNoxA is essential for these functions. Finally, we elucidate the role of BcNoxD and BcNoxB inside the ER by complementing the deletion mutants with ER bound alleles.

Conclusions

This study provides a deeper analysis of the Nox complexes in B. cinerea. Besides new insights in the overall regulation of the complexes, we provide further evidence that the NoxA complex has a predominant role inside the ER, while the NoxB complex is mainly important outside the ER, likely at the plasma membrane. By considering all other putative Nox complex members, we propose a putative model, which describes the distinct complex pattern upon certain differentiation processes.

SUBMITTER: Marschall R

PROVIDER: S-EPMC5611593 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Publications

Update on Nox function, site of action and regulation in <i>Botrytis cinerea</i>.

Marschall Robert R Siegmund Ulrike U Burbank Joachim J Tudzynski Paul P

Fungal biology and biotechnology 20161007

<h4>Background</h4>The production of reactive oxygen species (ROS) and a balanced redox homeostasis are essential parameters, which control the infection process of the plant pathogen <i>Botrytis cinerea</i>. The necrotrophic fungus is able to cope with the plants' oxidative burst and even produces its own ROS to overcome the plants' defense barrier. Major enzyme complexes, which are responsible for the production of superoxide, are NADPH oxidase (Nox) complexes. They play a central role in vari ...[more]

PMID: 28955467

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Project description:The plant hormone cytokinin (CK) is an important developmental regulator. Previous work has demonstrated that CKs mediate plant immunity and disease resistance. Some phytopathogens have been reported to secrete CKs and may manipulate CK signaling to improve pathogenesis. In recent work, we demonstrated that CK directly inhibits the development and virulence of fungal phytopathogens by attenuating the cell cycle and reducing cytoskeleton organization. Here, focusing on Botrytis cinerea, we report that CK possesses a dual role in fungal biology, with role prioritization being based on sugar availability. In a sugar-rich environment, CK strongly inhibited B. cinerea growth and deregulated cytoskeleton organization. This effect diminished as sugar availability decreased. In its second role, we show using biochemical assays and transgenic redox-sensitive fungal lines that CK can promote glycolysis and energy consumption in B. cinerea, both in vitro and in planta. Glycolysis and increased oxidation mediated by CK were stronger in low sugar availability, indicating that sugar availability could indeed be one possible element determining the role of CK in the fungus. Transcriptomic data further support our findings, demonstrating significant upregulation to glycolysis, oxidative phosphorylation, and sucrose metabolism upon CK treatment. Thus, the effect of CK in fungal biology likely depends on energy status. In addition to the plant producing CK during its interaction with the pathogen for defense priming and pathogen inhibition, the pathogen may take advantage of this increased CK to boost its metabolism and energy production, in preparation for the necrotrophic phase of the infection. IMPORTANCE The hormone cytokinin (CK) is a plant developmental regulator. Previous research has highlighted the involvement of CK in plant defense. Here, we report that CK has a dual role in plant-fungus interactions, inhibiting fungal growth while positively regulating B. cinerea energy utilization, causing an increase in glucose utilization and energy consumption. The effect of CK on B. cinerea was dependent on sugar availability, with CK primarily causing increases in glycolysis when sugar availability was low, and growth inhibition in a high-sugar environment. We propose that CK acts as a signal to the fungus that plant tissue is present, causing it to activate energy metabolism pathways to take advantage of the available food source, while at the same time, CK is employed by the plant to inhibit the attacking pathogen.