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Title: Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbling mode

Author
item GUI, C - Shanghai Institutes For Biological Sciences
item DONG, X - Shanghai Institutes For Biological Sciences
item LIU, H - Shanghai Institutes For Biological Sciences
item HUANG, W - Shanghai Institutes For Biological Sciences
item BARBERINI, M - University Of Buenos Aires
item GAO, X - Shanghai Institutes For Biological Sciences
item MUSCHIETTI, J - University Of Buenos Aires
item McCormick, Sheila
item TANG, W - Shanghai Institutes For Biological Sciences

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/15/2014
Publication Date: 9/5/2014
Citation: Gui, C., Dong, X., Liu, H., Huang, W., Barberini, M.L., Gao, X., Muschietti, J., Mccormick, S.M., Tang, W. 2014. Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbling mode. The Plant Cell. 26:3538-3555.

Interpretive Summary: Pollen tubes grow by extension from the tip. Here we show that overexpressing a receptor kinase called LePRK1 causes pollen tubes to change their growth pattern from the normal tube shape to one which formed blebs from the enlarged tip. We show that the blebbing can be suppressed by co-expressing other proteins at the same time, such as proteins that bind to actin, a plant cytoskeleton protein, or to the kinase itself.

Technical 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 (LePRK1DECD) 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 Ca2+-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 LePRK1DECD 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 LePRK1DECD 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 LePRK1DECD, 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.