Phosphatidic Acid Counteracts S-RNase Signaling in Pollen by Stabilizing the Actin Cytoskeleton

Abstract

S-RNase is the female determinant of self-incompatibility (SI) in pear (). After translocation to the pollen tube, S-RNase degrades rRNA and induces pollen tube death in an -haplotype-specific manner. In this study, we found that the actin cytoskeleton is a target of S-RNase (PbrS-RNase) and uncovered a mechanism that involves phosphatidic acid (PA) and protects the pollen tube from PbrS-RNase cytotoxicity. PbrS-RNase interacts directly with PbrActin1 in an -haplotype-independent manner, causing the actin cytoskeleton to depolymerize and promoting programmed cell death in the self-incompatible pollen tube. Pro-156 of PbrS-RNase is essential for the PbrS-RNase-PbrActin1 interaction, and the actin cytoskeleton-depolymerizing function of PbrS-RNase does not require its RNase activity. PbrS-RNase cytotoxicity enhances the expression of phospholipase D (PbrPLDδ1), resulting in increased PA levels in the incompatible pollen tube. PbrPLDδ1-derived PA initially prevents depolymerization of the actin cytoskeleton elicited by PbrS-RNase and delays the SI signaling that leads to pollen tube death. This work provides insights into the orchestration of the S-RNase-based SI response, in which increased PA levels initially play a protective role in incompatible pollen, until sustained PbrS-RNase activity reaches the point of no return and pollen tube growth ceases.

In-Depth Understanding of Camellia oleifera Self-Incompatibility by Comparative Transcriptome, Proteome and Metabolome

“…The GSI of Solanaceae, Scrophulariaceae and Rosaceae are regulated by S-RNase, which are determined by pistil-specific expression of S-RNase and pollen-specific expression of S-locus F-box protein (SLF/SFB) [18][19][20]. S-RNase can affect the degradation of pollen tube RNA and depolymerize the cytoskeleton, resulting in the occurrence of programmed cell death (PCD) in the pollen tube in Pyrus bretschneideri [21]. As S-RNase possesses cytotoxicity, it seems that S-RNase may trigger signaling pathways or defense responses following its entry into the pollen tube [21][22][23].…”

RNA-Seq analysis of compatible and incompatible styles of Pyrus species at the beginning of pollination

“…In the self-incompatibility of Pyrus , arresting incompatible pollen tube growth requires mechanisms that are partly similar to the SI response of poppy (Wang & Zhang, 2011). In the process of GSI in Pyrus , the S-RNase in the style enters the pollen tube and induces PCD in the incompatible pollen tube (Chen et al , 2018; Wang et al , 2010a). There were only two genes related to PCD according to the high-throughout sequencing data, and the difference in expression of the two genes reached significant levels ( P <0.05) only 2 h after pollination (Table 7).…”

Live and Let Die: Phosphatidic Acid Modulates the Self-Incompatibility Response

“…While RNA degradation has a wellestablished role in SI, the authors report that pear (Pyrus bretschneideri) S-RNases also have actin filament binding and severing activities that promote SI cytotoxicity (see figure; Chen et al, 2018). This finding links S-RNases to an actin destabilization phenomenon widely observed in SI pollen tubes.…”

“…To optimize genetic diversity, nearly half of all flowering plant species have developed a strategy known as self-incompatibility (SI) that selectively arrests growth of closely related (incompatible) pollen tubes while allowing passage of unrelated (compatible) donors (Fujii et al, 2016). In this issue, Chen et al (2018) identify a protective mechanism that uses phosphatidic acid (PA) to delay the effects of SI cytotoxicity.…”