{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T06:23:20Z","timestamp":1788330200218,"version":"build-2803163510"},"reference-count":67,"publisher":"Wiley","issue":"8","license":[{"start":{"date-parts":[[2025,6,20]],"date-time":"2025-06-20T00:00:00Z","timestamp":1750377600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32170335"],"award-info":[{"award-number":["32170335"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32300572"],"award-info":[{"award-number":["32300572"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010905","name":"Major Research Plan","doi-asserted-by":"publisher","award":["92254303"],"award-info":[{"award-number":["92254303"]}],"id":[{"id":"10.13039\/501100010905","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["JIPB"],"published-print":{"date-parts":[[2025,8]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Phosphatidylinositol 4,5\u2010bisphosphate (PI(4,5)P<jats:sub>2<\/jats:sub>) is known to be an instrumental anionic phospholipid in governing pollen germination and pollen tube growth. However, the precise functions and regulatory mechanisms of PI(4,5)P<jats:sub>2<\/jats:sub> in pollen polarity establishment and germination remain poorly understood. Our previous studies demonstrated the pivotal involvement of <jats:italic>Arabidopsis<\/jats:italic> formin homology 5 (AtFH5)\u2010dependent vesicle trafficking in polarity establishment of pollen. Here, we observed that PI(4,5)P<jats:sub>2<\/jats:sub> accumulated and oscillated at the prospective germination site, a process closely associated with the rotational movement of AtFH5\u2010labeled vesicles. Disruption of the mobility of AtFH5\u2010labeled vesicles, either through AtFH5 mutation or pharmacological treatment, significantly perturbed the accumulation of PI(4,5)P<jats:sub>2<\/jats:sub> at the plasma membrane. Subcellular localization and genetic analysis revealed that two phosphatidylinositol 4\u2010phosphate 5\u2010kinases, AtPIP5K1 and AtPIP5K4, are essential for PI(4,5)P<jats:sub>2<\/jats:sub> oscillation at the germination site prior to pollen germination. Furthermore, we found that the dynamics of AtPIP5K4 depended on the mobility of AtFH5\u2010labeled vesicles and reduced PI(4,5)P<jats:sub>2<\/jats:sub> in turn disturbed the attachment of AtFH5\u2010labeled secretory vesicles to the plasma membrane. In conclusion, these findings collectively highlight the reciprocal regulation of AtFH5\u2010labeled secretory vesicles and PI(4,5)P<jats:sub>2<\/jats:sub> oscillations at the plasma membrane, providing critical insights into the molecular mechanism underlying polarity establishment during pollen germination.<\/jats:p>","DOI":"10.1111\/jipb.13945","type":"journal-article","created":{"date-parts":[[2025,6,20]],"date-time":"2025-06-20T08:15:13Z","timestamp":1750407313000},"page":"2229-2244","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Reciprocal regulation between AtFH5\u2010labeled secretory vesicles and PI(4,5)P<sub>2<\/sub> oscillation at the plasma membrane directs pollen germination"],"prefix":"10.1111","volume":"67","author":[{"ORCID":"https:\/\/orcid.org\/0009-0003-6667-1886","authenticated-orcid":false,"given":"Yuwan","family":"Zhao","sequence":"first","affiliation":[{"name":"Center for Biological Science and Technology, Zhuhai\u2010Macao Biotechnology Joint Laboratory Beijing Normal University at Zhuhai Zhuhai 519087 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-8026-6881","authenticated-orcid":false,"given":"Zijing","family":"Huang","sequence":"additional","affiliation":[{"name":"Center for Biological Science and Technology, Zhuhai\u2010Macao Biotechnology Joint Laboratory Beijing Normal University at Zhuhai Zhuhai 519087 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1741-6657","authenticated-orcid":false,"given":"Ting","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Science Beijing Normal University Beijing 100875 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4801-800X","authenticated-orcid":false,"given":"Yi","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Science Beijing Normal University Beijing 100875 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6111-3063","authenticated-orcid":false,"given":"Zhufeng","family":"Chen","sequence":"additional","affiliation":[{"name":"Center for Biological Science and Technology, Zhuhai\u2010Macao Biotechnology Joint Laboratory Beijing Normal University at Zhuhai Zhuhai 519087 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4935-1026","authenticated-orcid":false,"given":"Yihao","family":"Li","sequence":"additional","affiliation":[{"name":"Center for Biological Science and Technology, Zhuhai\u2010Macao Biotechnology Joint Laboratory Beijing Normal University at Zhuhai Zhuhai 519087 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2164-0678","authenticated-orcid":false,"given":"Haiyun","family":"Ren","sequence":"additional","affiliation":[{"name":"Center for Biological Science and Technology, Zhuhai\u2010Macao Biotechnology Joint Laboratory Beijing Normal University at Zhuhai Zhuhai 519087 China"},{"name":"Key Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Science Beijing Normal University Beijing 100875 China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2025,6,20]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"crossref","DOI":"10.1038\/srep11454","article-title":"Cortical actin networks induce spatio\u2010temporal confinement of phospholipids in the plasma membrane\u2010a minimally invasive investigation by STED\u2010FCS","volume":"5","author":"Andrade D.M.","year":"2015","journal-title":"Sci. Rep."},{"key":"e_1_2_9_3_1","doi-asserted-by":"crossref","first-page":"1499","DOI":"10.1038\/s41556-022-00997-7","article-title":"Spatiotemporal dynamics of membrane surface charge regulates cell polarity and migration","volume":"24","author":"Banerjee T.","year":"2022","journal-title":"Nat. Cell Biol."},{"key":"e_1_2_9_4_1","first-page":"980","article-title":"Exocyst SEC. 3 and phosphoinositides define sites of exocytosis in pollen tube initiation and growth","volume":"172","author":"Bloch D.","year":"2016","journal-title":"Plant Physiol."},{"key":"e_1_2_9_5_1","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.molcel.2018.08.005","article-title":"Structural basis for regulation of phosphoinositide kinases and their involvement in human disease","volume":"71","author":"Burke J.E.","year":"2018","journal-title":"Mol. Cell"},{"key":"e_1_2_9_6_1","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.pbi.2020.05.007","article-title":"Signaling phospholipids in plant development: Small couriers determining cell fate","volume":"57","author":"Champeyroux C.","year":"2020","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_7_1","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.plaphy.2015.06.010","article-title":"Bisphenol A affects germination and tube growth in Picea meyeri pollen through modulating Ca2+ flux and disturbing actin\u2010dependent vesicular trafficking during cell wall construction","volume":"94","author":"Chang T.","year":"2015","journal-title":"Plant Physiol. Biochem."},{"key":"e_1_2_9_8_1","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1146\/annurev.arplant.59.032607.092921","article-title":"Structural and signaling networks for the polar cell growth machinery in pollen tubes","volume":"59","author":"Cheung A.Y.","year":"2008","journal-title":"Annu. Rev. Plant Biol."},{"key":"e_1_2_9_9_1","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1016\/j.pbi.2006.09.014","article-title":"Polarized growth: Maintaining focus on the tip","volume":"9","author":"Cole R.A.","year":"2006","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_10_1","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1083\/jcb.200909025","article-title":"An electrostatic switch displaces phosphatidylinositol phosphate kinases from the membrane during phagocytosis","volume":"187","author":"Fairn G.D.","year":"2009","journal-title":"J. Cell Biol."},{"key":"e_1_2_9_11_1","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1093\/plcell\/koaa035","article-title":"Plasma membrane nano\u2010organization specifies phosphoinositide effects on Rho\u2010GTPases and actin dynamics in tobacco pollen tubes","volume":"33","author":"Fratini M.","year":"2021","journal-title":"Plant Cell"},{"key":"e_1_2_9_12_1","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.immuni.2018.08.017","article-title":"PIP5 kinases regulate membrane phosphoinositide and actin composition for targeted granule secretion by cytotoxic lymphocytes","volume":"49","author":"Gawden\u2010Bone C.M.","year":"2018","journal-title":"Immunity"},{"key":"e_1_2_9_13_1","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1146\/annurev-arplant-042916-041022","article-title":"Guilt by association: A phenotype\u2010based view of the plant phosphoinositide network","volume":"68","author":"Gerth K.","year":"2017","journal-title":"Annu. Rev. Plant Biol."},{"key":"e_1_2_9_14_1","doi-asserted-by":"crossref","DOI":"10.1083\/jcb.202010077","article-title":"Lipid anchoring and electrostatic interactions target NOT\u2010LIKE\u2010DAD to pollen endo\u2010plasma membrane","volume":"220","author":"Gilles L.M.","year":"2021","journal-title":"J. Cell Biol."},{"key":"e_1_2_9_15_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.pbi.2023.102365","article-title":"Connecting the plant cytoskeleton to the cell surface via the phosphoinositides","volume":"73","author":"Goldy C.","year":"2023","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_16_1","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1016\/j.cell.2012.05.008","article-title":"Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules","volume":"149","author":"Gowrishankar K.","year":"2012","journal-title":"Cell"},{"key":"e_1_2_9_17_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.pbi.2022.102257","article-title":"Protein polarization: Spatiotemporal precisions in cell division and differentiation","volume":"68","author":"Guo X.","year":"2022","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_18_1","doi-asserted-by":"crossref","first-page":"15013","DOI":"10.1073\/pnas.1901744116","article-title":"Stochastic geometry sensing and polarization in a lipid kinase\u2010phosphatase competitive reaction","volume":"116","author":"Hansen S.D.","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_2_9_19_1","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.73747","article-title":"Membrane\u2010mediated dimerization potentiates PIP5K lipid kinase activity","volume":"11","author":"Hansen S.D.","year":"2022","journal-title":"eLife"},{"key":"e_1_2_9_20_1","doi-asserted-by":"crossref","first-page":"4053","DOI":"10.1038\/sj.emboj.7601834","article-title":"Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane","volume":"26","author":"He B.","year":"2007","journal-title":"EMBO J."},{"key":"e_1_2_9_21_1","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1016\/j.bbalip.2014.09.018","article-title":"Plant phosphoinositides\u2010complex networks controlling growth and adaptation","volume":"1851","author":"Heilmann M.","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"e_1_2_9_22_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.pbi.2022.102218","article-title":"Regulators regulated: Different layers of control for plasma membrane phosphoinositides in plants","volume":"67","author":"Heilmann M.","year":"2022","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_23_1","doi-asserted-by":"crossref","first-page":"3519","DOI":"10.1105\/tpc.106.047373","article-title":"Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling","volume":"18","author":"Helling D.","year":"2006","journal-title":"Plant Cell"},{"key":"e_1_2_9_24_1","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1146\/annurev.cellbio.17.1.159","article-title":"Polarized cell growth in higher plants","volume":"17","author":"Hepler P.K.","year":"2001","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"e_1_2_9_25_1","doi-asserted-by":"crossref","first-page":"3312","DOI":"10.1105\/tpc.108.059568","article-title":"Type B phosphatidylinositol\u20104\u2010phosphate 5\u2010kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion","volume":"20","author":"Ischebeck T.","year":"2008","journal-title":"Plant Cell"},{"key":"e_1_2_9_26_1","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1093\/mp\/ssq031","article-title":"Functional cooperativity of enzymes of phosphoinositide conversion according to synergistic effects on pectin secretion in tobacco pollen tubes","volume":"3","author":"Ischebeck T.","year":"2010","journal-title":"Mol. Plant"},{"key":"e_1_2_9_27_1","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1016\/j.celrep.2017.07.041","article-title":"Vesicle docking Is a key target of local PI(4,5)P2 metabolism in the secretory pathway of INS\u20101 cells","volume":"20","author":"Ji C.","year":"2017","journal-title":"Cell Rep."},{"key":"e_1_2_9_28_1","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1111\/tpj.16490","article-title":"Redundant function of the Arabidopsis phosphatidylinositol 4\u2010phosphate 5\u2010kinase genes PIP5K4\u20106 is essential for pollen germination","volume":"117","author":"Kato M.","year":"2023","journal-title":"Plant J."},{"key":"e_1_2_9_29_1","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1016\/j.tplants.2019.08.005","article-title":"Molecular basis of pollen germination in cereals","volume":"24","author":"Kim Y.\u2010J.","year":"2019","journal-title":"Trends Plant Sci."},{"key":"e_1_2_9_30_1","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1105\/tpc.107.056119","article-title":"The Arabidopsis phosphatidylinositol phosphate 5\u2010kinase PIP5K3 is a key regulator of root hair tip growth","volume":"20","author":"Kusano H.","year":"2008","journal-title":"Plant Cell"},{"key":"e_1_2_9_31_1","doi-asserted-by":"crossref","DOI":"10.1038\/srep40279","article-title":"Exocyst subunit SEC3A marks the germination site and is essential for pollen germination in Arabidopsis thaliana","volume":"7","author":"Li Y.","year":"2017","journal-title":"Sci. Rep."},{"key":"e_1_2_9_32_1","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1007\/s00425-013-1938-5","article-title":"\u03b3\u2010Aminobutyric acid (GABA) homeostasis regulates pollen germination and polarized growth in Picea wilsonii","volume":"238","author":"Ling Y.","year":"2013","journal-title":"Planta"},{"key":"e_1_2_9_33_1","doi-asserted-by":"crossref","first-page":"1389","DOI":"10.1016\/j.molp.2018.09.004","article-title":"Actin polymerization mediated by AtFH5 directs the polarity establishment and vesicle trafficking for pollen germination in Arabidopsis","volume":"11","author":"Liu C.","year":"2018","journal-title":"Mol. Plant"},{"key":"e_1_2_9_34_1","doi-asserted-by":"crossref","first-page":"1252","DOI":"10.1093\/plcell\/koab027","article-title":"Profilin promotes formin\u2010mediated actin filament assembly and vesicle transport during polarity formation in pollen","volume":"33","author":"Liu C.","year":"2021","journal-title":"Plant Cell"},{"key":"e_1_2_9_35_1","doi-asserted-by":"crossref","first-page":"4483","DOI":"10.1091\/mbc.e07-05-0461","article-title":"Phosphatidylinositol 4,5\u2010bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells","volume":"18","author":"Liu J.","year":"2007","journal-title":"Mol. Biol. Cell"},{"key":"e_1_2_9_36_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2022.04.089","article-title":"A mechanism for exocyst\u2010mediated tethering via Arf6 and PIP5K1C\u2010driven phosphoinositide conversion","volume":"32","author":"Maib H.","year":"2022","journal-title":"Curr. Biol."},{"key":"e_1_2_9_37_1","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.devcel.2019.11.015","article-title":"Plasma membrane domain patterning and self\u2010reinforcing polarity in Arabidopsis","volume":"52","author":"Marhava P.","year":"2020","journal-title":"Dev. Cell"},{"key":"e_1_2_9_38_1","doi-asserted-by":"crossref","first-page":"2557","DOI":"10.1523\/JNEUROSCI.3761-04.2005","article-title":"Plasmalemmal phosphatidylinositol\u20104,5\u2010bisphosphate level regulates the releasable vesicle pool size in chromaffin cells","volume":"25","author":"Milosevic I.","year":"2005","journal-title":"J. Neurosci."},{"key":"e_1_2_9_39_1","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1104\/pp.004770","article-title":"Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide\u2010specific phospholipase C","volume":"130","author":"Mueller\u2010Roeber B.","year":"2002","journal-title":"Plant Physiol."},{"key":"e_1_2_9_40_1","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1146\/annurev-cellbio-100818-125211","article-title":"Plant cell polarity: Creating diversity from inside the box","volume":"35","author":"Muroyama A.","year":"2019","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"e_1_2_9_41_1","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.pbi.2017.06.017","article-title":"Precision targeting by phosphoinositides: How PIs direct endomembrane trafficking in plants","volume":"40","author":"Noack L.C.","year":"2017","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_42_1","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1146\/annurev-arplant-081519-035910","article-title":"Functions of anionic lipids in plants","volume":"71","author":"Noack L.C.","year":"2020","journal-title":"Annu. Rev. Plant Biol."},{"key":"e_1_2_9_43_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2023.112036","article-title":"Local PI(4,5)P2 signaling inhibits fusion pore expansion during exocytosis","volume":"42","author":"Omar\u2010Hmeadi M.","year":"2023","journal-title":"Cell Rep."},{"key":"e_1_2_9_44_1","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1111\/j.1365-313X.2010.04168.x","article-title":"Mutual regulation of plant phospholipase D and the actin cytoskeleton","volume":"62","author":"Pleskot R.","year":"2010","journal-title":"Plant J."},{"key":"e_1_2_9_45_1","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1111\/nph.12814","article-title":"Live\u2010cell imaging of phosphatidic acid dynamics in pollen tubes visualized by Spo20p\u2010derived biosensor","volume":"203","author":"Potocky M.","year":"2014","journal-title":"New Phytol."},{"key":"e_1_2_9_46_1","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1083\/jcb.200508116","article-title":"A role for the RabA4b effector protein PI\u20104Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana","volume":"172","author":"Preuss M.L.","year":"2006","journal-title":"J. Cell Biol."},{"key":"e_1_2_9_47_1","doi-asserted-by":"crossref","first-page":"1665","DOI":"10.1105\/tpc.19.00970","article-title":"Specific recruitment of phosphoinositide species to the plant\u2010pathogen interfacial membrane underlies Arabidopsis susceptibility to fungal infection","volume":"32","author":"Qin L.","year":"2020","journal-title":"Plant Cell"},{"key":"e_1_2_9_48_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2023.113319","article-title":"AtFH5\u2010labeled secretory vesicles\u2010dependent calcium oscillation drives exocytosis and stepwise bulge during pollen germination","volume":"42","author":"Ruan H.","year":"2023","journal-title":"Cell Rep."},{"key":"e_1_2_9_49_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2020.609600","article-title":"Regulation of exocyst function in pollen tube growth by phosphorylation of exocyst subunit EXO70C2","volume":"11","author":"Saccomanno A.","year":"2020","journal-title":"Front. Plant Sci."},{"key":"e_1_2_9_50_1","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1146\/annurev-cellbio-111315-125349","article-title":"Phosphoinositides in control of membrane dynamics","volume":"32","author":"Schink K.O.","year":"2016","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"e_1_2_9_51_1","doi-asserted-by":"crossref","first-page":"1659","DOI":"10.1104\/pp.16.01709","article-title":"Analysis of exocyst subunit EXO70 family reveals distinct membrane polar domains in tobacco pollen tubes","volume":"173","author":"Sekeres J.","year":"2017","journal-title":"Plant Physiol."},{"key":"e_1_2_9_52_1","doi-asserted-by":"crossref","first-page":"E8977","DOI":"10.1073\/pnas.1705032114","article-title":"Mechanistic principles underlying regulation of the actin cytoskeleton by phosphoinositides","volume":"114","author":"Senju Y.","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_2_9_53_1","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1111\/tpj.12358","article-title":"A multi\u2010colour\/multi\u2010affinity marker set to visualize phosphoinositide dynamics in Arabidopsis","volume":"77","author":"Simon M.L.A.","year":"2013","journal-title":"Plant J."},{"key":"e_1_2_9_54_1","doi-asserted-by":"crossref","first-page":"3050","DOI":"10.1105\/tpc.108.058826","article-title":"Arabidopsis phosphatidylinositol\u20104\u2010monophosphate 5\u2010kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling","volume":"20","author":"Sousa E.","year":"2008","journal-title":"Plant Cell"},{"key":"e_1_2_9_55_1","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1105\/tpc.107.052852","article-title":"The type B phosphatidylinositol\u20104\u2010phosphate 5\u2010kinase 3 is essential for root hair formation in Arabidopsis thaliana","volume":"20","author":"Stenzel I.","year":"2008","journal-title":"Plant Cell"},{"key":"e_1_2_9_56_1","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1038\/s41477-024-01818-5","article-title":"The peri\u2010germ cell membrane: Poorly characterized but key interface for plant reproduction","volume":"10","author":"Sugi N.","year":"2024","journal-title":"Nat. Plants"},{"key":"e_1_2_9_57_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2105287118","article-title":"Plasma membrane phospholipid signature recruits the plant exocyst complex via the EXO70A1 subunit","volume":"118","author":"Synek L.","year":"2021","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_2_9_58_1","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1146\/annurev.arplant.48.1.461","article-title":"Pollen germination and tube growth","volume":"48","author":"Taylor L.P.","year":"1997","journal-title":"Annu. Rev. Plant Physiol. Plant Mol. Biol."},{"key":"e_1_2_9_59_1","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.plantsci.2016.05.014","article-title":"Phosphatidylinositol 4\u2010phosphate 5\u2010kinases 1 and 2 are involved in the regulation of vacuole morphology during Arabidopsis thaliana pollen development","volume":"250","author":"Ugalde J.M.","year":"2016","journal-title":"Plant Sci."},{"key":"e_1_2_9_60_1","doi-asserted-by":"crossref","first-page":"1692","DOI":"10.1104\/pp.105.069765","article-title":"Effects of brefeldin A on pollen germination and tube growth. Antagonistic effects on endocytosis and secretion","volume":"139","author":"Wang Q.","year":"2005","journal-title":"Plant Physiol."},{"key":"e_1_2_9_61_1","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1093\/pcp\/pcac025","article-title":"Functional differentiation among the Arabidopsis phosphatidylinositol 4\u2010phosphate 5\u2010kinase genes PIP5K1, PIP5K2 and PIP5K3","volume":"63","author":"Watari M.","year":"2022","journal-title":"Plant Cell Physiol."},{"key":"e_1_2_9_62_1","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/S1369-5266(98)80046-0","article-title":"Signaling tip growth in plants","volume":"1","author":"Yang Z.","year":"1998","journal-title":"Curr. Opin. Plant Biol."},{"key":"e_1_2_9_63_1","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms14236","article-title":"Sec. 3 promotes the initial binary t\u2010SNARE complex assembly and membrane fusion","volume":"8","author":"Yue P.","year":"2017","journal-title":"Nat. Commun."},{"key":"e_1_2_9_64_1","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1083\/jcb.200704128","article-title":"Membrane association and functional regulation of Sec. 3 by phospholipids and Cdc42","volume":"180","author":"Zhang X.","year":"2008","journal-title":"J. Cell Biol."},{"key":"e_1_2_9_65_1","doi-asserted-by":"crossref","first-page":"2200","DOI":"10.1104\/pp.109.142349","article-title":"Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes","volume":"152","author":"Zhang Y.","year":"2010","journal-title":"Plant Physiol."},{"key":"e_1_2_9_66_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.gene.2020.144915","article-title":"Genome\u2010wide systematic characterization and expression analysis of the phosphatidylinositol 4\u2010phosphate 5\u2010kinases in plants","volume":"756","author":"Zhang Z.","year":"2020","journal-title":"Gene"},{"key":"e_1_2_9_67_1","doi-asserted-by":"crossref","first-page":"4031","DOI":"10.1105\/tpc.110.076760","article-title":"Phosphoinositides regulate clathrin\u2010dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco","volume":"22","author":"Zhao Y.","year":"2010","journal-title":"Plant Cell"},{"key":"e_1_2_9_68_1","doi-asserted-by":"crossref","first-page":"3170","DOI":"10.1105\/tpc.19.00844","article-title":"The tip\u2010localized phosphatidylserine established by Arabidopsis ALA3 Is crucial for Rab GTPase\u2010mediated vesicle trafficking and pollen tube growth","volume":"32","author":"Zhou Y.","year":"2020","journal-title":"Plant Cell"}],"container-title":["Journal of Integrative Plant Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/jipb.13945","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,8,1]],"date-time":"2025-08-01T11:36:49Z","timestamp":1754048209000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/jipb.13945"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,20]]},"references-count":67,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2025,8]]}},"alternative-id":["10.1111\/jipb.13945"],"URL":"https:\/\/doi.org\/10.1111\/jipb.13945","archive":["Portico"],"relation":{},"ISSN":["1672-9072","1744-7909"],"issn-type":[{"value":"1672-9072","type":"print"},{"value":"1744-7909","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,20]]},"assertion":[{"value":"2024-12-19","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-05-06","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-06-20","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}