title: Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbing mode.
abstract: The tubular growth of a pollen tube cell is crucial for the sexual reproduction of flowering plants. LePRK1 is a pollen-specific and plasma membrane-localized receptor-like kinase from tomato (Solanum lycopersicum). LePRK1 interacts with another receptor, LePRK2, and with KINASE PARTNER PROTEIN (KPP), a Rop guanine nucleotide exchange factor. Here, we show that pollen tubes overexpressing LePRK1 or a truncated LePRK1 lacking its extracellular domain (LePRK1ΔECD) have enlarged tips but also extend their leading edges by producing "blebs." Coexpression of LePRK1 and tomato PLIM2a, an actin bundling protein that interacts with KPP in a Ca(2+)-responsive manner, suppressed these LePRK1 overexpression phenotypes, whereas pollen tubes coexpressing KPP, LePRK1, and PLIM2a resumed the blebbing growth mode. We conclude that overexpression of LePRK1 or LePRK1ΔECD rewires pollen tube growth to a blebbing mode, through KPP- and PLIM2a-mediated bundling of actin filaments from tip plasma membranes. Arabidopsis thaliana pollen tubes expressing LePRK1ΔECD also grew by blebbing. Our results exposed a hidden capability of the pollen tube cell: upon overexpression of a single membrane-localized molecule, LePRK1 or LePRK1ΔECD, it can switch to an alternative mechanism for extension of the leading edge that is analogous to the blebbing growth mode reported for Dictyostelium and for Drosophila melanogaster stem cells.
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Cai-Ping
authors.initials: CP
authors.lastname: Gui
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Xin
authors.initials: X
authors.lastname: Dong
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Hai-Kuan
authors.initials: HK
authors.lastname: Liu
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Wei-Jie
authors.initials: WJ
authors.lastname: Huang
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Dong
authors.initials: D
authors.lastname: Zhang
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Shu-Jie
authors.initials: SJ
authors.lastname: Wang
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Dr. Hector Torres, C1428ADN Buenos Aires, Argentina.
authors.forename: María Laura
authors.initials: ML
authors.lastname: Barberini
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Xiao-Yan
authors.initials: XY
authors.lastname: Gao
authors.affiliation: Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Dr. Hector Torres, C1428ADN Buenos Aires, Argentina Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EGA Buenos Aires, Argentina.
authors.forename: Jorge
authors.initials: J
authors.lastname: Muschietti
authors.affiliation: Plant Gene Expression Center, U.S. Department of Agriculture/Agricultural Research Service, and Department of Plant and Microbial Biology, University of California at Berkeley, Albany, California 94710.
authors.forename: Sheila
authors.initials: S
authors.lastname: McCormick
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China Plant Gene Expression Center, U.S. Department of Agriculture/Agricultural Research Service, and Department of Plant and Microbial Biology, University of California at Berkeley, Albany, California 94710 whtang@sibs.ac.cn.
authors.forename: Wei-Hua
authors.identifier: http://orcid.org/0000-0002-6167-7870
authors.initials: WH
authors.lastname: Tang
mesh_terms: D000199:Actins / Q000378:metabolism; D022081:Cell Surface Extensions / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D018525:Germination; D018551:Solanum lycopersicum / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development*; D010641:Phenotype; D010940:Plant Proteins / Q000737:chemistry / Q000378:metabolism*; D030821:Plants, Genetically Modified; D053205:Pollen Tube / Q000201:enzymology* / Q000254:growth & development* / Q000648:ultrastructure; D011485:Protein Binding; D021381:Protein Transport
chemical_list: D000199:Actins; D010940:Plant Proteins