Fumonisin B1-Induced Oxidative Burst Perturbed Photosynthetic Activity and Affected Antioxidant Enzymatic Response in Tomato Plants in Ethylene-Dependent Manner

Abstract

Fumonisin B1 (FB1) is a harmful mycotoxin produced by Fusarium species, which results in oxidative stress leading to cell death in plants. FB1 perturbs the metabolism of sphingolipids and causes growth and yield reduction. This study was conducted to assess the role of ethylene in the production and metabolism of reactive oxygen species in the leaves of wild type (WT) and ethylene receptor mutant Never ripe (Nr) tomato and to elucidate the FB1-induced phytotoxic effects on the photosynthetic activity and antioxidant mechanisms triggered by FB1 stress. FB1 exposure resulted in significant ethylene emission in a concentration-dependent manner in both genotypes. Moreover, FB1 significantly affected the photosynthetic parameters of PSII and PSI and activated photoprotective mechanisms, such as non-photochemical quenching in both genotypes, especially under 10 µM FB1 concentration. Further, the net photosynthetic rate and stomatal conductance were significantly reduced in both genotypes in a FB1 dose-dependent manner. Interestingly, lipid peroxidation and loss of cell viability were also more pronounced in WT as compared to Nr leaves indicating the role of ethylene in cell death induction in the leaves. Thus, FB1-induced oxidative stress affected the working efficiency of PSI and PSII in both tomato genotypes. However, ethylene-dependent antioxidant enzymatic defense mechanisms were activated by FB1 and showed significantly elevated levels of superoxide dismutase (18.6%), ascorbate peroxidase (129.1%), and glutathione S-transferase activities (66.62%) in Nr mutants as compared to WT tomato plants confirming the role of ethylene in the regulation of cell death and defense mechanisms under the mycotoxin exposure.

Trichothecenes and Fumonisins: Key Players in Fusarium–Cereal Ecosystem Interactions

“…Beyond cereals and Arabidopsis, more recent studies on fruits such as tomatoes and bananas have also increased our understanding of the cellular impacts of FB1. A study on tomatoes determined that ethylene plays an important role in the regulation of FB1-mediated cell death and defence activation, significantly affecting photosystems I and II and activating photoprotective mechanisms [ 28 ]. In bananas, FB1 biosynthesis by F. proliferatum contributed to fungal infection by decreasing plant defence, enhancing oxidative stress and ROS production, regulating energy metabolism and accelerating cell death [ 29 , 30 ].…”

“…Ethylene signalling is an important factor in sphingolipid synthesis, and it has been shown to partially rescue FB1-induced cell death in tomatoes in Arabidopsis [ 28 , 52 ]. Relatively few studies have elucidated maize mechanisms that confer tolerance to fumonisins.…”

Role of Plant defence system in crop protection against Fusarium pathogens

“…OH), and singlet oxygen ( 1 O 2 ) [15]. These antioxidants include superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), polyphenol oxidase (PPO), ascorbate peroxidase (APX), ascorbate (ASA), and glutathione (GSH) and perform scavenging function of ROS production during pathogenic attacks [17,26].…”

Fusaric acid-evoked oxidative stress affects plant defence system by inducing biochemical changes at subcellular level

“…In addition, cell death plays an essential role in the coordination of plant growth and development, as well as in the induction of cellular responses to various stresses (Valandro et al 2020 ). Plants induce cell death at the infection site to prevent further spread of pathogen infection and toxin production (Iqbal et al 2022 ; Xing et al 2013 ). Saffron root tip cells were exposed to 25–200 µM FA for 60 h, and it was observed that FA induced higher H 2 O 2 accumulation, chromatin condensation and DNA breakage followed by cell death (Samadi and Shahsavan Behboodi 2006 ).…”