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Arabidopsis PCaP2 modulates the phosphatidylinositol 4,5-bisphosphate signal on the plasma membrane and attenuates root hair elongation.
Plant J. 2019 08; 99(4):610-625.PJ

Abstract

Phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2 ] serves as a subcellular signal on the plasma membrane, mediating various cell-polarized phenomena including polar cell growth. Here, we investigated the involvement of Arabidopsis thaliana PCaP2, a plant-unique plasma membrane protein with phosphoinositide-binding activity, in PtdIns(4,5)P2 signaling for root hair tip growth. The long-root-hair phenotype of the pcap2 knockdown mutant was found to stem from its higher average root hair elongation rate compared with the wild type and to counteract the low average rate caused by a defect in the PtdIns(4,5)P2 -producing enzyme gene PIP5K3. On the plasma membrane of elongating root hairs, the PCaP2 promoter-driven PCaP2-green fluorescent protein (GFP), which complemented the pcap2 mutant phenotype, overlapped with the PtdIns(4,5)P2 marker 2xCHERRY-2xPHPLC in the subapical region, but not at the apex, suggesting that PCaP2 attenuates root hair elongation via PtdIns(4,5)P2 signaling on the subapical plasma membrane. Consistent with this, a GFP fusion with the PCaP2 phosphoinositide-binding domain PCaP2N23 , root hair-specific overexpression of which caused a low average root hair elongation rate, localized more intense to the subapical plasma membrane than to the apical plasma membrane similar to PCaP2-GFP. Inducibly overexpressed PCaP2-GFP, but not its derivative lacking the PCaP2N23 domain, replaced 2xCHERRY-2xPHPLC on the plasma membrane in root meristematic epidermal cells, and suppressed FM4-64 internalization in elongating root hairs. Moreover, inducibly overexpressed PCaP2 arrested an endocytic process of PIN2-GFP recycling. Based on these results, we conclude that PCaP2 functions as a negative modulator of PtdIns(4,5)P2 signaling on the subapical plasma membrane probably through competitive binding to PtdIns(4,5)P2 and attenuates root hair elongation.

Authors+Show Affiliations

Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan.Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan.Laboratory of Cell Dynamics, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Nagoya, Aichi, 464-8601, Japan.Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

30604455

Citation

Kato, Mariko, et al. "Arabidopsis PCaP2 Modulates the Phosphatidylinositol 4,5-bisphosphate Signal On the Plasma Membrane and Attenuates Root Hair Elongation." The Plant Journal : for Cell and Molecular Biology, vol. 99, no. 4, 2019, pp. 610-625.
Kato M, Tsuge T, Maeshima M, et al. Arabidopsis PCaP2 modulates the phosphatidylinositol 4,5-bisphosphate signal on the plasma membrane and attenuates root hair elongation. Plant J. 2019;99(4):610-625.
Kato, M., Tsuge, T., Maeshima, M., & Aoyama, T. (2019). Arabidopsis PCaP2 modulates the phosphatidylinositol 4,5-bisphosphate signal on the plasma membrane and attenuates root hair elongation. The Plant Journal : for Cell and Molecular Biology, 99(4), 610-625. https://doi.org/10.1111/tpj.14226
Kato M, et al. Arabidopsis PCaP2 Modulates the Phosphatidylinositol 4,5-bisphosphate Signal On the Plasma Membrane and Attenuates Root Hair Elongation. Plant J. 2019;99(4):610-625. PubMed PMID: 30604455.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Arabidopsis PCaP2 modulates the phosphatidylinositol 4,5-bisphosphate signal on the plasma membrane and attenuates root hair elongation. AU - Kato,Mariko, AU - Tsuge,Tomohiko, AU - Maeshima,Masayoshi, AU - Aoyama,Takashi, Y1 - 2019/02/15/ PY - 2018/08/24/received PY - 2018/12/12/revised PY - 2018/12/17/accepted PY - 2019/1/4/pubmed PY - 2020/6/9/medline PY - 2019/1/4/entrez KW - 5-bisphosphate KW - PCaP2 KW - cell polarity KW - membrane signal KW - phosphatidylinositol 4 KW - phosphatidylinositol phosphate 5-kinase KW - root hair elongation SP - 610 EP - 625 JF - The Plant journal : for cell and molecular biology JO - Plant J. VL - 99 IS - 4 N2 - Phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2 ] serves as a subcellular signal on the plasma membrane, mediating various cell-polarized phenomena including polar cell growth. Here, we investigated the involvement of Arabidopsis thaliana PCaP2, a plant-unique plasma membrane protein with phosphoinositide-binding activity, in PtdIns(4,5)P2 signaling for root hair tip growth. The long-root-hair phenotype of the pcap2 knockdown mutant was found to stem from its higher average root hair elongation rate compared with the wild type and to counteract the low average rate caused by a defect in the PtdIns(4,5)P2 -producing enzyme gene PIP5K3. On the plasma membrane of elongating root hairs, the PCaP2 promoter-driven PCaP2-green fluorescent protein (GFP), which complemented the pcap2 mutant phenotype, overlapped with the PtdIns(4,5)P2 marker 2xCHERRY-2xPHPLC in the subapical region, but not at the apex, suggesting that PCaP2 attenuates root hair elongation via PtdIns(4,5)P2 signaling on the subapical plasma membrane. Consistent with this, a GFP fusion with the PCaP2 phosphoinositide-binding domain PCaP2N23 , root hair-specific overexpression of which caused a low average root hair elongation rate, localized more intense to the subapical plasma membrane than to the apical plasma membrane similar to PCaP2-GFP. Inducibly overexpressed PCaP2-GFP, but not its derivative lacking the PCaP2N23 domain, replaced 2xCHERRY-2xPHPLC on the plasma membrane in root meristematic epidermal cells, and suppressed FM4-64 internalization in elongating root hairs. Moreover, inducibly overexpressed PCaP2 arrested an endocytic process of PIN2-GFP recycling. Based on these results, we conclude that PCaP2 functions as a negative modulator of PtdIns(4,5)P2 signaling on the subapical plasma membrane probably through competitive binding to PtdIns(4,5)P2 and attenuates root hair elongation. SN - 1365-313X UR - https://www.unboundmedicine.com/medline/citation/30604455/Arabidopsis_PCaP2_modulates_the_phosphatidylinositol_45_bisphosphate_signal_on_the_plasma_membrane_and_attenuates_root_hair_elongation_ L2 - https://doi.org/10.1111/tpj.14226 DB - PRIME DP - Unbound Medicine ER -