Early events induced by the toxin deoxynivalenol lead to programmed cell death in Nicotiana tabacum cells

Abstract

Deoxynivalenol (DON) is a mycotoxin affecting animals and plants. This toxin synthesized by Fusarium culmorum and Fusarium graminearum is currently believed to play a decisive role in the fungal phytopathogenesis as a virulence factor. Using cultured cells of Nicotiana tabacum BY2, we showed that DON-induced programmed cell death (PCD) could require transcription and translation processes, in contrast to what was observed in animal cells. DON could induce different cross-linked pathways involving (i) reactive oxygen species (ROS) generation linked, at least partly, to a mitochondrial dysfunction and a transcriptional down-regulation of the alternative oxidase (Aox1) gene and (ii) regulation of ion channel activities participating in cell shrinkage, to achieve PCD.

Mycotoxin‐assisted mitochondrial dysfunction and cytotoxicity: Unexploited tools against proliferative disorders

“…In mouse thymic epithelial cell line 1 (MTEC1), deoxynivalenol increased ROS production and changed mitochondrial membrane potential leading to apoptotic cell death via activation of caspase‐3, caspase‐8, caspase‐9 and poly(ADP‐ribose) polymerase (PARP) . Moreover, in Nicotiana tabacum BY2 cultured cells, this mycotoxin induced programmed cell death possibly by inducing ROS and causing mitochondrial dysfunction, which led to transcriptional downregulation of the alternative oxidase ( Aox1 ) gene and regulation of ion channel activities participating in cell shrinkage .…”

“…Mitochondria are the main sources of ROS/RNS, and these can damage cellular lipids, proteins, and DNA . Oosporein , citrinin , ochratoxin A , T‐2 toxin , gliotoxin , and deoxynivalenol were found to augment ROS, leading to mitochondrial dysfunction by increasing oxidative stress in the test systems. Accumulation of ROS and downregulation of physiological antioxidant has a dual effect of oxidative stress.…”

Ion Transport in Plant Cell Shrinkage During Death

“…An increase in K + outward rectifying conductances (KORC) was recorded in response to various CD-inducing microbederived molecules, such as harpins (El-Maarouf et al, 2001;Haapalainen et al, 2012), deoxinivalenol (DON) (Yekkour et al, 2015) or CD-inducing ROS stress (Demidchik et al, 2010(Demidchik et al, , 2014, like ozone (Tran et al, 2013a). Conductances with different activation kinetics and selectivity (Demidchik et al, 2014) are likely triggered by GORK or SKOR channels (Tran et al, 2013a;Demidchik et al, 2014), but could also be provoked by annexins, cyclic nucleotide-gated channels and ionotropic glutamate receptors.…”

“…Conductances with different activation kinetics and selectivity (Demidchik et al, 2014) are likely triggered by GORK or SKOR channels (Tran et al, 2013a;Demidchik et al, 2014), but could also be provoked by annexins, cyclic nucleotide-gated channels and ionotropic glutamate receptors. Nonetheless, the use of K + channel blockers decreases KORC, CD-extent (Haapalainen et al, 2012), cell shrinkage (Yekkour et al, 2015) or even activation of metacaspases (Tran et al, 2013a), proteases and endonucleases (Demidchik et al, 2014(Demidchik et al, , 2018. Recently, gork1-1 mutants lacking K + efflux channel were also shown to have fewer autophagosomes compared to the wild-type plant upon ROS-induced CD (Demidchik, 2018).…”

“…In response to ozone or DON, plant cells rapidly activate anion currents, followed by a delayed activation of KORC (Tran et al, 2013a;Yekkour et al, 2015), the whole ion efflux being thus transiently not electroneutral. Such increases in anion currents were also recorded with other CD-inducing microbederived molecules, such as harpins (Reboutier et al, 2007), fusaric acid (Bouizgarne et al, 2006), oxalic acid (Errakhi et al, 2008), cryptogein (Gauthier et al, 2007), or with ozone (Kadono et al, 2010), drought (Dauphin et al, 2001) or hydroxyl radicals (Pottosin et al, 2018).…”