The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death

Abstract

SummaryThe mitochondrion has emerged as a key regulator of apoptosis, a form of animal programmed cell death (PCD). The mitochondrial permeability transition (MPT), facilitated by a pore-mediated, rapid permeability increase in the inner membrane, has been implicated as an early and critical step of apoptosis. Victorin, the host-selective toxin produced by Cochliobolus victoriae, the causal agent of victoria blight of oats, has been demonstrated to bind to the mitochondrial P-protein and also induces a form of PCD. Previous results suggest that a MPT may facilitate victorin's access to the mitochondrial matrix and binding to the P-protein: (i) victorin-induced cell death displays features similar to apoptosis; (ii) in vivo, victorin binds to the mitochondrial P-protein only in toxin-sensitive genotypes whereas victorin binds equally well to P-protein isolated from toxin-sensitive and insensitive oats; (iii) isolated, untreated mitochondria are impermeable to victorin. The data implicate an in vivo change in mitochondrial permeability in response to victorin. This study focused on whether oat mitochondria can undergo a MPT. Isolated oat mitochondria demonstrated high-amplitude swelling when treated with spermine or Ca 2+ in the presence of the Ca 2+ -ionophore A23187, and when treated with mastoparan, an inducer of the MPT in rat liver mitochondria. In all cases, swelling demonstrated size exclusion in the range 0.9±1.7 kDa, similar to that found in animal mitochondria. Further, MPT-inducing conditions permitted victorin access to the mitochondrial matrix and binding to the P-protein. In vivo, victorin treatment induced the collapse of mitochondrial transmembrane potential within 2 h, indicating a MPT. Also, the victorin-induced collapse of membrane potential was clearly distinct from that induced by uncoupling respiration, as the latter event prevented the victorin-induced PCD response and binding to P-protein. These results demonstrate that a MPT can occur in oat mitochondria in vitro, and are consistent with the hypothesis that an MPT, which allows victorin access to the mitochondrial matrix and binding to the P-protein, occurs in vivo during victorin-induced PCD.

Thioredoxinh5 Is Required for Victorin Sensitivity Mediated by a CC-NBS-LRR Gene inArabidopsis

“…This is in direct contrast with the action of ATTRX5, which acts as a positive regulator of victorininduced cell death. Victorin triggers a programmed cell death response in sensitive oats that resembles apoptosis (Navarre and Wolpert, 1999;Yao et al, 2001Yao et al, , 2002Curtis and Wolpert, 2002;Coffeen and Wolpert, 2004), and this also appears to be true in sensitive Arabidopsis (T.A. Sweat, unpublished results).…”

ACAULIS5 controlsArabidopsisxylem specification through the prevention of premature cell death

“…An analogous mechanism was proposed for polyamines in the regulation of mitochondrial integrity, which is central to apoptotic cell death in animals (Tassani et al, 1995). In this context, it is interesting to note that spermine has been shown to inhibit mitochondrial membrane permeability in oats (Curtis and Wolpert, 2002).…”

Mitochondrial Respiratory Deficiencies Signal Up-regulation of Genes for Heat Shock Proteins

“…To test directly whether genes for mitochondrial and cytosolic HSPs respond to increases in cytosolic Ca 2ϩ , we treated B37T maize seedlings with the ionophore A23187, which causes fluxes of intracompartmental Ca 2ϩ into the cytosol. Unlike methomyl, which would also release Ca 2ϩ specifically from mitochondria (40), A23187 does not affect ⌬ m unless exogenous Ca 2ϩ is supplied (41,42).…”