Role of the Actin Cytoskeleton in Self-Incompatibility

Chen et.al. demonstrate that phosphatidic acid mitigates S-RNase signaling in pollen by stabilizing the actin cytoskeleton. Plant Cell (2018). https://doi.org/10.1105/tpc.18.00021

By Jianqing Chen, Peng Wang, Shaoling Zhang, and Juyou Wu

Background: The success of sexual reproduction in flowering plants is entirely dependent on communication between pollen (carrying male gametes) and the pistil (female organ of flower). To prevent self-fertilization and promote outbreeding in the wild, self-incompatibility (SI) exists in many plants. SI allows the pistil of a plant to reject only pollen originating from the same plant or pollen from plant that carries the same SI genotype. The most widespread form of SI operates through a pistil-expressed S-RNase mechanism. Following pollination and pollen germination, S-RNases are translocated to the growing pollen tube, where the activity of incompatible S-RNases eventually leads to pollen tube death. Fertilization is critical for plant breeding and food production. Self-incompatibility leads to the need for artificial pollination in pear production, which is both labor- and cost-intensive.

Question: Besides degrading RNA, are there other targets for S-RNase in the pollen tube? How does the pollen tube against the cytotoxicity of S-RNase?

Findings: We found that the actin cytoskeleton is a target of S-RNase in pear and uncovered a mechanism that protects the pollen tube from S-RNase cytotoxicity involving phosphatidic acid. Pear S-RNase interacts directly with the actin protein, causing the actin cytoskeleton to depolymerize and promoting programmed cell death in the self-incompatible pollen tube. S-RNase also increases phosphatidic acid levels in the incompatible pear pollen tube, which initially play a protective role, until sustained S-RNase activity reaches the point of no return and pollen tube death.

Next steps: We have observed that the actin cytoskeleton is a target of S-RNase in pear; thus, we are investigating the possibility of overcoming self-incompatibility by stabilizing the actin cytoskeleton in pear production.

Jianqing Chen, Peng Wang, Barend H.J. de Graaf, Hao Zhang, Huijun Jiao, Chao Tang, Shaoling Zhang, Juyou Wu (2018). Phosphatidic Acid Counteracts S-RNase Signaling in Pollen by Stabilizing the Actin Cytoskeleton. Plant Cell May 2018, 30: 1023-1039; DOI: https://doi.org/10.1105/tpc.18.00021