Plant proteases during developmental programmed cell death

Abstract

Proteases are among the key regulators of most forms of programmed cell death (PCD) in animals. Many PCD processes have also been associated with protease expression or activation in plants, However, functional evidence for the roles and actual modes of action of plant proteases in PCD remains surprisingly limited. In this review, we provide an update on protease involvement in the context of developmentally regulated plant PCD. To illustrate the diversity of protease functions, we focus on several prominent developmental PCD processes, including xylem and tapetum maturation, suspensor elimination, endosperm degradation, and seed coat formation, as well as plant senescence processes. Despite the substantial advances in the field, protease functions are often only correlatively linked to developmental PCD, and the specific molecular roles of proteases in many developmental PCD processes remain to be elucidated.

Keywords: Developmental PCD (dPCD); development; plant; programmed cell death (PCD); protease; protein degradation.

Figure 1. Hypothetical regulatory network of the plant dPCD process.

Coordinated with cellular differentiation, dPCD competency is achieved at least partly on the transcriptional level. A range of PCD-associated genes are upregulated, and their proteins accumulate in cells that are preparing to undergo PCD. Once competent, a hypothetical trigger starts the PCD execution process. Finally, partial or complete corpse clearance is achieved by activity of degrading enzymes that are activated during PCD and complete corpse clearance post mortem. Conceivably, proteases might play roles in all of these steps, but so far only few protease functions in dPCD have been characterized in detail.

Figure 2. Proteases implicated in selected PCD processes occurring during plant development.

PCD processes are an integral part of vegetative and reproductive plant development. They occur during xylem and tapetum differentiation, in various tissues during seed development and germination, and during plant organ senescence. We indicate proteases that have been implicated with aspects of these cell death processes in the individual tissues. For some of the PCD processes listed, no functional data for protease involvement exists to date. Abbreviations are: A, aleurone layer; E, endosperm; ESR, embryo-surrounding region of the endosperm; I, seed integuments; S, suspensor.

Figure 3. Selection of dPCD-associated proteases with known or predicted subcellular localizations.

Many dPCD-associated proteases accumulate as inactive proenzymes or in specific subcellular compartments before they are activated. Especially the vacuole, but also the ER and ER-derived vesicles can serve as storage space for inactive proteases. Once PCD execution is triggered, the breakup of cellular compartments is thought to release these proteases into the same compartments as their targets. The specific chemical environment of subcellular compartments before and after compartment breakup can be an additional cue to activate PCD-associated proteases. Abbreviations are: A, apoplast; C, cell wall; Ch, chloroplast; ER, endoplasmic reticulum; M, mitochondrion; N, nucleus; PM, plasma membrane; R, ricinosome; V, vacuole.