https://www.cell.com/trends/plant-science/pdf/S1360-1385(15)00203-4.pdf

Licensed to Kill: Mitochondria, Chloroplasts, and Cell Death

Plants are frequently exposed to different stressful factors, both of biotic or abiotic nature, which limit their growth and productivity. To survive under stress conditions, plants must activate stress-specific signalling pathways, which finally lead to morphological, physiological, and biochemical changes that allow to adapt to the adverse environment. Cellular redox homeostasis, determined by a complex interplay between pathways that produce and scavenge reactive oxygen species (ROS), plays a key role in the adaptive response. Each deviation in the cellular redox state, due to an imbalance of ROS production and/or scavenging, is indicative of environmental disturbance and works as a signal. Under stress conditions, different ROS are produced in many cell compartments. Plants have very proficient, versatile and flexible antioxidant machinery, which comprises enzymes and metabolites with distinct biochemical properties and distinct sub-cellular localization. The antioxidant systems play a key role in the control of redox homeostasis, determining either the extent or the specificity of ROS signals and the downstream redox-dependent responses. Redox signalling is responsive to a number of environmental cues, and the complex and dynamic pathways of redox regulation occur in different cell compartments. The redox-dependent modification of sensitive signalling proteins is proposed as a key mode of redox signal transmission. Each redox-dependent interaction is opportunely regulated by a restricted environment, whose change transfers the complex system of information and influences the plant response to external changes.

Redox State as a Central Regulator of Plant-Cell Stress Responses

Cytochrome c (CYTc) is a soluble redox-active heme protein that transfers electrons from complex III to complex IV in the cyanide-sensitive mitochondrial respiratory pathway. CYTc biogenesis is a complex process that requires multiple steps until the mature active protein is obtained. CYTc levels and activity are finely regulated, revealing the importance of this protein not only as electron carrier but also in many other processes. In this article, we describe the role of CYTc in mitochondrial respiration, from its canonical role as electron carrier for ATP production to its involvement in protein import and the stabilization of respiratory complexes and supercomplexes. In plants, CYTc is connected to the synthesis of the antioxidant ascorbate and the detoxification of toxic compounds. Finally, CYTc is also a multi-functional signaling molecule that influences the balance between life and death, acting in energy provision for cellular functions or triggering programmed cell death. The confluence of several metabolic routes into a single protein that links redox reactions with energy producing pathways seems logical from the point of view of cellular economy, control and organization.

Cytochrome c, a hub linking energy, redox, stress and signaling pathways in mitochondria and other cell compartments

Programmed cell death (PCD) is an integral cellular program by which targeted cells culminate to demise under certain developmental and pathological conditions. It is essential for controlling cell number, removing unwanted diseased or damaged cells and maintaining the cellular homeostasis. The details of PCD process has been very well elucidated and characterized in animals but similar understanding of the process in plants has not been achieved rather the field is still in its infancy that sees some sporadic reports every now and then. The plants have 2 energy generating sub-cellular organelles- mitochondria and chloroplasts unlike animals that just have mitochondria. The presence of chloroplast as an additional energy transducing and ROS generating compartment in a plant cell inclines to advocate the involvement of chloroplasts in PCD execution process. As chloroplasts are supposed to be progenies of unicellular photosynthetic organisms that evolved as a result of endosymbiosis, the possibility of retaining some of the components involved in bacterial PCD by chloroplasts cannot be ruled out. Despite several excellent reviews on PCD in plants, there is a void on an update of information at a place on the regulation of PCD by chloroplast. This review has been written to provide an update on the information supporting the involvement of chloroplast in PCD process and the possible future course of the field.

Programmed cell death in plants: A chloroplastic connection

Recent evidence has proved that caspase protease activities are detected in both mammals and plants during programmed cell death (PCD). The characteristics and functions of caspase-like proteases play important roles in understanding the mechanisms of PCD in plants. In this work, we report firstly the involvement of caspase-like protease activities and effects in aluminum (Al) stress in two contrasting peanut genotypes. Caspase-like activities in the root tip cells of ‘Zhonghua 2’ (Al-sensitive) and ‘99-1507’ (Al-tolerant) were detected using synthetic caspase substrates during Al-triggered PCD. Caspase-1-, -2-, -3-, -4-, -5-, -6-, -8- and -9-like proteases were found in peanut root tip cells. VDQQDase (caspase-2-like) and WEHD (caspase-5-like) were the first detected in the plants, and almost all of the caspase-like proteases were activated during Al-induced PCD, especially caspase-3-like and caspase-1-like, which was higher in ‘Zhonghua 2’ than in ‘99-1507’. The highest activity levels of caspase-3- and caspase-1-like proteases occurred 8 and 4 h after 100 µM Al treatment, respectively. Compared with 100 µM AlCl3 treatment alone, specific caspase-3 protease inhibitor Ac-DEVD-CHO inhibited the increase of caspase-3-like protease activity, Al content, Hsr203j expression, cell death and DNA fragmentation, and the decrease in root growth induced by 100 µM AlCl3 treatment, but it was more obvious in ‘Zhonghua 2’ than in ‘99-1507’. In conclusion, there were different caspase-like proteases in root tips of peanut, and caspase-3-like protease was a crucial executioner in Al-induced PCD. Its effects in the ‘Zhonghua 2’ genotype were higher than in ‘99-1507’. An improved model of the mechanism of Al-induced PCD and Al tolerance differences in different genotypes is proposed.

Caspase-like proteases regulate aluminum-induced programmed cell death in peanut

It has been known that the process of leaf senescence is accompanied by programmed cell death (PCD), and the previous study indicated that dark-induced senescence in detached leaves from rice led to the release of cytochrome f (Cyt f) from chloroplast into the cytoplasm. In this study, the effects of Cyt f on PCD were studied both in vitro and in vivo. In a cell-free system, purified Cyt f activated caspase-3-like protease and endonuclease OsNuc37, and induced DNA fragmentation. Furthermore, Cyt f-induced caspase-3-like activity could be inhibited by MG132, which suggests that the activity was attributed to the 26S proteasome. Conditional expression of Cyt f in the cytoplasm could also activate caspase-3-like activity and DNA fragmentation. Fluorescein diacetate staining and annexin V-FITC/PI double staining demonstrated that Cyt f expression in cytoplasm significantly increased the percentage of PCD protoplasts. Yeast two-hybrid screening showed that Cyt f might interact with E3-ubiquitin ligase and RPN9b, the subunits of the ubiquitin proteasome system (UPS), and other PCD-related proteins. Taken together, these results suggest that the released Cyt f from the chloroplast into the cytoplasm might activate or rescue caspase-3-like activity by interacting with the UPS, ultimately leading to the induction of PCD.

/pdf/induction-of-caspase-3-like-activity-in-rice-following-1997ducgzo.pdf

Induction of Caspase-3-like activity in Rice following release of cytochrome-f from the chloroplast and subsequent interaction with the Ubiquitin-Proteasome System

Huan Li

Papers

Induction of Caspase-3-like activity in Rice following release of cytochrome-f from the chloroplast and subsequent interaction with the Ubiquitin-Proteasome System