OsVPE3 Mediates GA-induced Programmed Cell Death in Rice Aleurone Layers via Interacting with Actin Microfilaments

Abstract

Background: Vacuolar processing enzymes (VPEs) have been identified as the enzymes that regulate vacuole-mediated programmed cell death (PCD) in plants. The mechanism that VPE regulates the PCD in rice aleurone layers remains unknown. Results: The aleurone layers treated with distilled water exerted caspase-1 and VPE activity, both of which were inhibited by the caspase-1 specific inhibitor Ac-YVAD-CMK but not by the caspase-3 specific inhibitor Ac-DEVD-CHO. However, the caspase-1 and caspase-3 inhibitors weakened the activity of caspase-3. Combined with the effects of endogenous gibberellin (GA) on the induction of OsVPEs, we suggest that the OsVPE3 in the aleurone layers, which exhibits caspase-1-like activity, is a key molecule in GA-induced PCD via regulating the protease with caspase-3-like activity. Many studies have confirmed that vacuolar fusion is an important feature of vacuole-mediated PCD in plants. In this experiment, the process of vacuole fusion was accompanied by changes in the structure of actin filaments (AFs), specifically, their depolymerization and polymerization. The process of vacuolar fusion was accelerated or delayed by the promotion or inhibition of the depolymerization of AFs, respectively. Here, the inhibition of OsVPE3 blocked the depolymerization of AFs and delayed the fusion of vacuoles, indicating that OsVPE3 can regulate the fusion of vacuoles in rice aleurone layers via mediating AFs. Furthermore, the depolymerization of AFs contributed to the up-regulation of OsVPE3 gene expression and VPE activity, resulting in accelerated PCD in rice aleurone layers. However, the inhibitor of VPE reversed the effects of AF depolymerization on the activity of VPE, then postponing the process of PCD, implying that AF can involve in GA-induced PCD of rice aleurone layers by mediating OsVPE3. Conclusions: Together, activation of OsVPE3 and depolymerization of AFs shortened the process of vacuolation and PCD in rice aleurone layers, and OsVPE3 interacted with AFs during regulation.

Meta-QTL analysis explores the key genes, especially hormone related genes, involved in the regulation of grain water content and grain dehydration rate in maize

“…The dead cells that had experienced PCD could promote the release of auxin (IAA) [ 8 ]. Gibberellin (GA) could also regulate the PCD process of the aleurone layer cells in the grain [ 9 ]. Increasing the level of ABA in maize grains had also been shown to accelerate the process of dehydration in the grains [ 10 ].…”

Unraveling the Molecular Functions of Multifaced Plant‐Vacuolar Processing Enzymes

“…In contrast, the inhibition of rice VPE blocked the depolymerization of actin filaments, which ultimately delayed the fusion of vacuoles, indicating the relation of vegetative type VPEs in mediating the actin filaments related PCD in aleurone layers. (Uemura et al, 2002;Zheng et al, 2017;Zhang et al, 2020). Moreover, abscisic acid (ABA) accumulates in the integument layers to delay aleurone vacuolation and induce seed dormancy (Bethke et al, 1999;Bethke et al, 2002;Bethke et al, 2007), whereas gibberellins (GA) promoted vacuolation to mobilize the reserve enzymes and compounds to incite aleurone PCD (Bethke et al, 2002;Zhang et al, 2020).…”

Vacuolar Processing Enzymes in Plant Programmed Cell Death and Autophagy

“…Primarily, it has been found that VPEs are responsible for the maturation of seed storage proteins such as 2S albumin and 12S globulin [ 20 ]. Now it is known that they participate in other developmental processes [ 21 , 22 , 23 , 24 , 25 , 26 ], senescence [ 27 , 28 , 29 ], and environmental stress responses [ 28 , 30 , 31 , 32 ]. During development, senescence, and plant responses to environmental stimuli, both autophagy [ 11 ] and PCD can be initiated [ 33 ].…”

“…Upregulation of VPEs occurs in various types of PCD. VPE involvement has been widely demonstrated during developmental PCD (dPCD), including seed coat formation in angiosperms [ 21 ], xylogenesis [ 23 ], development of the root velamen radicum in the epiphytic orchid Cymbidium tracyanum [ 25 ], development of pollen and tapetal cell degradation in Arabidopsis thaliana [ 24 , 26 ], leaf morphogenesis of the lace plant ( Aponogeton madagascariensis ) [ 34 ], and degradation of aleurone layers in rice ( Oryza sativa ) [ 22 , 30 ]. One of the best-known types of PCD regulated by VPEs is the hypersensitive response (HR), which was first observed in VPE-silenced Nicotiana benthamiana infected with tobacco mosaic virus (TMV) [ 35 ].…”

“…One of the best-known types of PCD regulated by VPEs is the hypersensitive response (HR), which was first observed in VPE-silenced Nicotiana benthamiana infected with tobacco mosaic virus (TMV) [ 35 ]. Furthermore, they take part in PCD induced by various abiotic stresses [ 19 , 28 , 30 , 36 , 37 , 38 , 39 ] and are even called executors of plant PCD. On the other hand, their role in the late stages of autophagy, i.e., degradation of autophagic bodies, is only presumed.…”