Acetylation of inorganic pyrophosphatase by S-RNase signaling induces pollen tube tip swelling by repressing pectin methylesterase

• Published in: The Plant cell 2023-09, Vol.35 (9), p.3544-3565
• Main Authors: Tang, Chao, Wang, Peng, Zhu, Xiaoxuan, Qi, Kaijie, Xie, Zhihua, Zhang, Hao, Li, Xiaoqiang, Gao, Hongru, Gu, Tingting, Gu, Chao, Li, Shan, de Graaf, Barend H J, Zhang, Shaoling, Wu, Juyou
• Format: Article
• Language: English
• Subjects: Acetylation; Inorganic Pyrophosphatase - genetics; Inorganic Pyrophosphatase - metabolism; Pollen Tube; Pyrus - metabolism; Ribonucleases - metabolism
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1093/plcell/koad162

Abstract Self-incompatibility (SI) is a widespread genetically determined system in flowering plants that prevents self-fertilization to promote gene flow and limit inbreeding. S-RNase–based SI is characterized by the arrest of pollen tube growth through the pistil. Arrested pollen tubes show disrupted polarized growth and swollen tips, but the underlying molecular mechanism is largely unknown. Here, we demonstrate that the swelling at the tips of incompatible pollen tubes in pear (Pyrus bretschneideri [Pbr]) is mediated by the SI-induced acetylation of the soluble inorganic pyrophosphatase (PPA) PbrPPA5. Acetylation at Lys-42 of PbrPPA5 by the acetyltransferase GCN5-related N-acetyltransferase 1 (GNAT1) drives accumulation of PbrPPA5 in the nucleus, where it binds to the transcription factor PbrbZIP77, forming a transcriptional repression complex that inhibits the expression of the pectin methylesterase (PME) gene PbrPME44. The function of PbrPPA5 as a transcriptional repressor does not require its PPA activity. Downregulating PbrPME44 resulted in increased levels of methyl-esterified pectins in growing pollen tubes, leading to swelling at their tips. These observations suggest a mechanism for PbrPPA5-driven swelling at the tips of pollen tubes during the SI response. The targets of PbrPPA5 include genes encoding cell wall–modifying enzymes, which are essential for building a continuous sustainable mechanical structure for pollen tube growth. In the self-incompatibility response, acetylation of PbrPPA5 enhances the repression of PbrPME44, resulting in the accumulation of methyl-esterified pectins of the pollen tube cell wall and tip swelling.