Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity.
Rapid tip growth allows for efficient development of highly elongated cells (e.g. neuronal axons, fungal hyphae and pollen tubes) and requires an elaborate spatiotemporal regulation of the growing region. Here, we use the pollen tube as a model to investigate the mechanism regulating the growing region. ROPs (Rho-related GTPases from plants) are essential for pollen tip growth and display oscillatory activity changes in the apical plasma membrane (PM). By manipulating the ROP activity level, we showed that the PM distribution of ROP activity as an apical cap determines the tip growth region and that efficient tip growth requires an optimum level of the apical ROP1 activity. Excessive ROP activation induced the enlargement of the tip growth region, causing growth depolarization and reduced tube elongation. Time-lapse analysis suggests that the apical ROP1 cap is generated by lateral propagation of a localized ROP activity. Subcellular localization and gain- and loss-of-function analyses suggest that RhoGDI- and RhoGAP-mediated global inhibition limits the lateral propagation of apical ROP1 activity. We propose that the balance between the lateral propagation and the global inhibition maintains an optimal apical ROP1 cap and generates the apical ROP1 activity oscillation required for efficient pollen-tube elongation.
Hwang
Jae-Ung
JU
Department of Botany and Plant Sciences and Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California-Riverside, Riverside, CA 92521, USA.
Wu
Guang
G
Yan
An
A
Lee
Yong-Jik
YJ
Grierson
Claire S
CS
Yang
Zhenbiao
Z
D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D019204:GTP-Binding Proteins / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000235:genetics / Q000502:physiology; D018613:Microscopy, Confocal; D030821:Plants, Genetically Modified / Q000201:enzymology / Q000235:genetics / Q000254:growth & development*; D053205:Pollen Tube / Q000201:enzymology / Q000235:genetics / Q000254:growth & development*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D020741:rho GTP-Binding Proteins / Q000235:genetics / Q000378:metabolism*
D029681:Arabidopsis Proteins; D019204:GTP-Binding Proteins; C501663:ROP1 protein, Arabidopsis; D020741:rho GTP-Binding Proteins