Turnover of diacylglycerol kinase 4 by cytoplasmic acidification induces vacuole morphological change and nuclear DNA degradation in the early stage of pear self‐incompatibility response

Abstract

Pear has an S‐RNase‐based gametophytic self‐incompatibility (SI) system. Nuclear DNA degradation is a typical feature of incompatible pollen tube death, and is among the many physiological functions of vacuoles. However, the specific changes that occur in vacuoles, as well as the associated regulatory mechanism in pear SI, are currently unclear. Although research in tobacco has shown that decreased activity of diacylglycerol kinase (DGK) results in the morphological change of pollen tube vacuole, whether DGK regulates the pollen tube vacuole of tree plants and whether it occurs in SI response, is currently unclear. We found that DGK activity is essential for pear pollen tube growth, and DGK4 regulates pollen tube vacuole morphology following its high expression and deposition at the tip and shank edge of the pollen tube of pear. Specifically, incompatible S‐RNase may induce cytoplasmic acidification of the pollen tube by inhibiting V‐ATPase V0 domain a1 subunit gene expression as early as 30 min after treatment, when the pollen tube is still alive. Cytoplasmic acidification induced by incompatible S‐RNase results in reduced DGK4 abundance and deposition, leading to morphological change of the vacuole and fragmentation of nuclear DNA, which indicates that DGK4 is a key factor in pear SI response.

Killing me softly - Programmed cell death in plant reproduction from sporogenesis to fertilization

“…In S-RNase-based SI, self-S-RNase exerts RNase toxicity and triggers a signaling cascade in the selfpollen, leading to tip-localized ROS disruption, actin cytoskeleton depolymerization, vacuole collapse, cytoplasmic pH decrease, caspase-like protease activation and nuclear DNA degradation, culminating in self-pollen tube PCD [50,51]. In poppy (Papaver rhoeas), SI is controlled by the female S-determinant PrsS (P. rhoeas stigma S), a small secreted stigma protein [52], and the male S-determinant PrpS (P. rhoeas pollen S), a pollen membrane protein [53].…”

Phase separation of S‐RNase promotes self‐incompatibility in Petunia hybrida

“…In Pyrus , S‐RNases interact directly with actin and cause the F‐actin to depolymerize, resulting in programmed cell death (PCD) of self‐pollen tubes (Chen et al, 2018). Tip‐localized reactive oxygen species (ROS) disruption and calcium ion level decreases were also observed during the SI response (Wang et al, 2010), and S‐RNase decreases diacylglycerol kinase 4 (DGK4) deposition resulting in the vacuole morphological changes (Kong et al, 2021). In Malus domestica , S‐RNase mediates F‐actin circulation imbalance and transfer RNA (tRNA) aminoacylation inhibition preventing self‐pollen tube growth in vitro (Li et al, 2018; Yang et al, 2018).…”

Phase separation of S-RNase promotes self-incompatibility inPetunia hybrida

“…In Pyrus , S-RNases interact directly with actin and cause the F-actin to depolymerize, resulting in programmed cell death (PCD) of self-pollen tubes (32). Tip-localized ROS disruption and calcium ions level decrease were also observed during the SI response (33), and S-RNase decreases diacylglycerol kinase 4 (DGK4) deposition resulting in the vacuole morphological changes (34). In Malus domestica , S-RNase mediates F-actin circulation imbalance and tRNA aminoacylation inhibition preventing self-pollen tube growth in vitro (35, 36).…”