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Self-incompatibility requires GPI anchor remodeling by the poppy PGAP1 ortholog HLD1

Zongcheng Lin (UGent) , Fei Xie, Marina Muñoz Triviño (UGent) , Tao Zhao, Frederik Coppens (UGent) , Lieven Sterck (UGent) , Maurice Bosch, Vernonica E. Franklin-Tong and Moritz Nowack (UGent)
(2022) CURRENT BIOLOGY. 32(9). p.1909-1923
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Abstract
Glycosylphosphatidylinositol-anchored proteins (GPI-APs) are tethered to the outer leaflet of the plasma membrane where they function as key regulators of a plethora of biological processes in eukaryotes. Self-incompatibility (SI) plays a pivotal role regulating fertilization in higher plants through recognition and rejection of "self" pollen. Here, we used Arabidopsis thaliana lines that were engineered to be self-incompatible by expression of Papaver rhoeas SI determinants for an SI suppressor screen. We identify HLD1/AtPGAP1, an ortholog of the human GPI-inositol deacylase PGAP1, as a critical component required for the SI response. Besides a delay in flowering time, no developmental defects were observed in HLD1/AtPGAP1 knockout plants, but SI was completely abolished. We demonstrate that HLD1/AtPGAP1 functions as a GPI-inositol deacylase and that this GPI-remodeling activity is essential for SI. Using GFP-SKU5 as a representative GPI-AP, we show that the HLD1/AtPGAP1 mutation does not affect GPI-AP production and targeting but affects their cleavage and release from membranes in vivo. Our data not only implicate GPI-APs in SI, providing new directions to investigate SI mechanisms, but also identify a key functional role for GPI-AP remodeling by inositol deacylation in planta.
Keywords
Arabidopsis, AtPGAP1, GPI-AP remodeling, GPI-inositol deacylase, HLD1, Papaver, pollen rejection, programmed cell death, self-incompatibility, General Biochemistry, Genetics and Molecular Biology, PROGRAMMED CELL-DEATH, GLYCOSYL-PHOSPHATIDYLINOSITOL, ARABINOGALACTAN-PROTEINS, ARABIDOPSIS-THALIANA, MEMBRANE-PROTEINS, FLOWERING PLANTS, PHOSPHOLIPASE-C, GROWTH, RECOGNITION, IDENTIFICATION

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Citation

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MLA
Lin, Zongcheng, et al. “Self-Incompatibility Requires GPI Anchor Remodeling by the Poppy PGAP1 Ortholog HLD1.” CURRENT BIOLOGY, vol. 32, no. 9, 2022, pp. 1909–23, doi:10.1016/j.cub.2022.02.072.
APA
Lin, Z., Xie, F., Muñoz Triviño, M., Zhao, T., Coppens, F., Sterck, L., … Nowack, M. (2022). Self-incompatibility requires GPI anchor remodeling by the poppy PGAP1 ortholog HLD1. CURRENT BIOLOGY, 32(9), 1909–1923. https://doi.org/10.1016/j.cub.2022.02.072
Chicago author-date
Lin, Zongcheng, Fei Xie, Marina Muñoz Triviño, Tao Zhao, Frederik Coppens, Lieven Sterck, Maurice Bosch, Vernonica E. Franklin-Tong, and Moritz Nowack. 2022. “Self-Incompatibility Requires GPI Anchor Remodeling by the Poppy PGAP1 Ortholog HLD1.” CURRENT BIOLOGY 32 (9): 1909–23. https://doi.org/10.1016/j.cub.2022.02.072.
Chicago author-date (all authors)
Lin, Zongcheng, Fei Xie, Marina Muñoz Triviño, Tao Zhao, Frederik Coppens, Lieven Sterck, Maurice Bosch, Vernonica E. Franklin-Tong, and Moritz Nowack. 2022. “Self-Incompatibility Requires GPI Anchor Remodeling by the Poppy PGAP1 Ortholog HLD1.” CURRENT BIOLOGY 32 (9): 1909–1923. doi:10.1016/j.cub.2022.02.072.
Vancouver
1.
Lin Z, Xie F, Muñoz Triviño M, Zhao T, Coppens F, Sterck L, et al. Self-incompatibility requires GPI anchor remodeling by the poppy PGAP1 ortholog HLD1. CURRENT BIOLOGY. 2022;32(9):1909–23.
IEEE
[1]
Z. Lin et al., “Self-incompatibility requires GPI anchor remodeling by the poppy PGAP1 ortholog HLD1,” CURRENT BIOLOGY, vol. 32, no. 9, pp. 1909–1923, 2022.
@article{8752988,
  abstract     = {{Glycosylphosphatidylinositol-anchored proteins (GPI-APs) are tethered to the outer leaflet of the plasma membrane where they function as key regulators of a plethora of biological processes in eukaryotes. Self-incompatibility (SI) plays a pivotal role regulating fertilization in higher plants through recognition and rejection of "self" pollen. Here, we used Arabidopsis thaliana lines that were engineered to be self-incompatible by expression of Papaver rhoeas SI determinants for an SI suppressor screen. We identify HLD1/AtPGAP1, an ortholog of the human GPI-inositol deacylase PGAP1, as a critical component required for the SI response. Besides a delay in flowering time, no developmental defects were observed in HLD1/AtPGAP1 knockout plants, but SI was completely abolished. We demonstrate that HLD1/AtPGAP1 functions as a GPI-inositol deacylase and that this GPI-remodeling activity is essential for SI. Using GFP-SKU5 as a representative GPI-AP, we show that the HLD1/AtPGAP1 mutation does not affect GPI-AP production and targeting but affects their cleavage and release from membranes in vivo. Our data not only implicate GPI-APs in SI, providing new directions to investigate SI mechanisms, but also identify a key functional role for GPI-AP remodeling by inositol deacylation in planta.}},
  author       = {{Lin, Zongcheng and Xie, Fei and Muñoz Triviño, Marina and Zhao, Tao and Coppens, Frederik and Sterck, Lieven and Bosch, Maurice and Franklin-Tong, Vernonica E. and Nowack, Moritz}},
  issn         = {{0960-9822}},
  journal      = {{CURRENT BIOLOGY}},
  keywords     = {{Arabidopsis,AtPGAP1,GPI-AP remodeling,GPI-inositol deacylase,HLD1,Papaver,pollen rejection,programmed cell death,self-incompatibility,General Biochemistry,Genetics and Molecular Biology,PROGRAMMED CELL-DEATH,GLYCOSYL-PHOSPHATIDYLINOSITOL,ARABINOGALACTAN-PROTEINS,ARABIDOPSIS-THALIANA,MEMBRANE-PROTEINS,FLOWERING PLANTS,PHOSPHOLIPASE-C,GROWTH,RECOGNITION,IDENTIFICATION}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{1909--1923}},
  title        = {{Self-incompatibility requires GPI anchor remodeling by the poppy PGAP1 ortholog HLD1}},
  url          = {{http://doi.org/10.1016/j.cub.2022.02.072}},
  volume       = {{32}},
  year         = {{2022}},
}
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