Alternative oxidase gene induced by nitric oxide is involved in the regulation of ROS and enhances the resistance of Pleurotus ostreatus to heat stress

Ludan Hou,Mengran Zhao,Lijiao Zhang,Chenyang Huang,Qi He,Jinxia Zhang

doi:10.1186/s12934-021-01626-y

Abstract

BackgroundIn China, during the cultivation process of Pleurotus ostreatus, the yield and quality of fruiting bodies are easily affected by high temperatures in summer. Nitric oxide (NO) plays an important regulatory role in the response to abiotic stress, and previous studies have found that NO can induce alternative oxidase (aox) experssion in response to heat stress (HS) by regulating aconitase. However, the regulatory pathway of NO is complex, and the function and regulation of the aox gene in the response to HS remain unclear.ResultsIn this study, we found that NO affected nicotinamide adenine dinucleotide (NADH) and adenosine triphosphate (ATP) levels, reduced hydrogen peroxide (H2O2) and superoxide anion (O2−) contents, and slowed O2− production. Further RNA-Seq results showed that NO regulated the oxidation-reduction process and oxidoreductase activity, affected the cellular respiration pathway and activated aox gene expression. The function of aox was determined by constructing overexpression (OE) and RNA interference (RNAi) strains. The results showed that the OE-aox strains exhibited obviously improved growth recovery after exposure to HS. During exposure to HS, the OE-aox strains exhibited reduced levels of NADH, the product of the tricarboxylic acid (TCA) cycle, and decreased synthesis of ATP, which reduced the production and accumulation of reactive oxygen species (ROS), whereas the RNAi-aox strains exhibited the opposite result. In addition, aox mediated the expression of antioxidant enzyme genes in the mycelia of P. ostreatus under HS through the retrograde signaling pathway.ConclusionsThis study shows that the expression of the aox gene in P. ostreatus mycelia can be induced by NO under HS, that it regulates the TCA cycle and cell respiration to reduce the production of ROS, and that it can mediate the retrograde signaling pathway involved in the mycelial response to HS.Graphical abstract

Highlights

In China, during the cultivation process of Pleurotus ostreatus, the yield and quality of fruiting bodies are affected by high temperatures in summer
The addition of exogenous Nitric oxide (NO) promoted the recovery of P. ostreatus mycelial growth after heat stress (HS), as shown in Fig. 1A. Hydrogen peroxide (H2O2) and O2− are important components of reactive oxygen species (ROS), and as shown in Fig. 1B, the content of H2O2 in mycelia increased significantly after HS (HS vs. control, P = 1.118 × 10− 6)
In summary, our data indicate that NO responds to HS by reducing the production and accumulation of ROS in P. ostreatus mycelia and can induce aox gene expression

Summary

Introduction

In China, during the cultivation process of Pleurotus ostreatus, the yield and quality of fruiting bodies are affected by high temperatures in summer. Nitric oxide (NO) plays an important regulatory role in the response to abiotic stress, and previous studies have found that NO can induce alternative oxidase (aox) experssion in response to heat stress (HS) by regulating aconitase. During the cultivation process of P. ostreatus, high temperatures in summer limit the growth of mycelia, the formation of primordia and the development of fruiting bodies, and thereby seriously affecting the yield. The mycelia response to changes in temperature is very complex and includes different physiological and metabolic changes that affect the overall development of edible fungi as well as interactions between cells and molecules. In recent years, increasing attention has been given to the mechanism through which fungi respond to HS

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