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Phosphatidic acid counteracts S-RNase signaling in pollen by stabilizing the actin cytoskeleton

Chen, Jianqing, Wang, Peng, De Graaf, Barend H. J., Zhang, Hao, Jiao, Huijun, Tang, Chao, Zhang, Shaoling and Wu, Juyou 2018. Phosphatidic acid counteracts S-RNase signaling in pollen by stabilizing the actin cytoskeleton. Plant Cell 30 (5) , pp. 1023-1039. 10.1105/tpc.18.00021

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S-RNase is the female determinant of self-incompatibility (SI) in pear (Pyrus bretschneideri). After translocation to the pollen tube, S-RNase degrades rRNA and induces pollen tube death in an S-haplotype-specific manner. In this study, we found that the actin cytoskeleton is a target of P. bretschneideri 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 S-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.

Item Type: Article
Date Type: Publication
Status: Published
Schools: Biosciences
Publisher: American Society of Plant Biologists
ISSN: 1040-4651
Date of First Compliant Deposit: 24 May 2018
Date of Acceptance: 27 April 2018
Last Modified: 08 Jun 2020 11:20

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