Vacuolar Processing Enzymes in Plant Programmed Cell Death and Autophagy

Abstract

Vacuolar processing enzymes (VPEs) are plant cysteine proteases that are subjected to autoactivation in an acidic pH. It is presumed that VPEs, by activating other vacuolar hydrolases, are in control of tonoplast rupture during programmed cell death (PCD). Involvement of VPEs has been indicated in various types of plant PCD related to development, senescence, and environmental stress responses. Another pathway induced during such processes is autophagy, which leads to the degradation of cellular components and metabolite salvage, and it is presumed that VPEs may be involved in the degradation of autophagic bodies during plant autophagy. As both PCD and autophagy occur under similar conditions, research on the relationship between them is needed, and VPEs, as key vacuolar proteases, seem to be an important factor to consider. They may even constitute a potential point of crosstalk between cell death and autophagy in plant cells. This review describes new insights into the role of VPEs in plant PCD, with an emphasis on evidence and hypotheses on the interconnections between autophagy and cell death, and indicates several new research opportunities.

Fertilization-induced synergid cell death by RALF12-triggered ROS production and ethylene signaling

“…The cysteine protease CEP1, for example, which is transported to the vacuole and transformed into a mature enzyme before rupture of the vacuole, functions as a key executor in tapetal PCD 48 . Vacuolar processing enzymes (VPEs), major vacuolar proteases with caspase-like activity, can activate other vacuolar hydrolases, and thus are in control of tonoplast rupture and vacuole collapse 2,49 . VPEs translocate to the vacuole through the autophagy pathway 50 , and autophagy is functionally implicated in corpse clearance during dPCD 51,52 .…”

Ac-DEVD-CHO (caspase-3/DEVDase inhibitor) suppresses self-incompatibility–induced programmed cell death in the pollen tubes of petunia (Petunia hybrida E. Vilm.)

“…During the final collapse, ricinosomes are disorganized to release the mature enzyme. Acidification of the cytoplasm disintegrates ricinosomes in vivo, which changes the tonoplast permeability at the late PCD stage [ 4 ].…”

“…The orthologs of many key animal apoptotic genes, including the genes coding for caspases, are absent in the plant genome; however, the proteases with a caspase-like enzyme activity were shown to be necessary for the plant PCD (for review, see ref. [ 3 , 4 ]). The role of caspase-3-like protease/DEVDase has been especially intensively studied; correspondingly, this enzyme activity is currently used as a PCD marker (for review, see ref.…”

Autophagy and Symbiosis: Membranes, ER, and Speculations

“…As a part of the response to pathogens, autophagy has been shown to regulate the disease-related cell death response, including the lytic clearance of the whole cell. Such strong immune response is an efficient strategy of an immobile organism, which allows it, at the expense of losing several cells, to restrict further infection [ 9 , 10 , 11 , 17 , 18 ].…”

“…Once the autophagosome fuses with the vacuole, their limiting membrane and contents are degraded by vacuolar hydrolases active against lipids, proteins, nucleic acids, and carbohydrates. Caspase-like vacuolar processing enzyme γ (VPE-γ), the prominent protease, activates a number of vacuolar zymogens [ 13 , 18 ]. Another type of autophagy in plant cells, mega-autophagy, is the cell autolysis and degradation during the process of programmed cell death (PCD) [ 12 , 13 ].…”