Receptor-like kinases as surface regulators for RAC/ROP-mediated pollen tube growth and interaction with the pistil

Abstract

Background: RAC/ROPs are RHO-type GTPases and are known to play diverse signalling roles in plants. Cytoplasmic RAC/ROPs are recruited to the cell membrane and activated in response to extracellular signals perceived and mediated by cell surface-located signalling assemblies, transducing the signals to regulate cellular processes. More than any other cell types in plants, pollen tubes depend on continuous interactions with an extracellular environment produced by their surrounding tissues as they grow within the female organ pistil to deliver sperm to the female gametophyte for fertilization.

Scope: We review studies on pollen tube growth that provide compelling evidence indicating that RAC/ROPs are crucial for regulating the cellular processes that underlie the polarized cell growth process. Efforts to identify cell surface regulators that mediate extracellular signals also point to RAC/ROPs being the molecular switches targeted by growth-regulating female factors for modulation to mediate pollination and fertilization. We discuss a large volume of work spanning more than two decades on a family of pollen-specific receptor kinases and some recent studies on members of the FERONIA family of receptor-like kinases (RLKs).

Significance: The research described shows the crucial roles that two RLK families play in transducing signals from growth regulatory factors to the RAC/ROP switch at the pollen tube apex to mediate and target pollen tube growth to the female gametophyte and signal its disintegration to achieve fertilization once inside the female chamber.

Fig. 1

RAC/ROP GTPase signalling of polarized pollen tube growth. (A) Regulation of the RAC/ROP molecular switch (modified from Nibau et al. 2006). (B) Apically located RAC/ROP switch in a pollen tube (modified from Cheung and Wu 2008).

Fig. 2

Cell membrane-located PRK regulates pollen tube tip growth. LAT52-GFP-Nt-PRK-transformed tobacco pollen tubes are shown. (A) Cell surface localization of GFP-Nt-PRK in elongating pollen tubes. Typical of pollen tube cell membrane-associated proteins, vesicles loaded with FP-PRKs also concentrate in and cycle rapidly in and out of the apical cytoplasm (see also Cheung et al. 2002), which is known to be occupied almost exclusively by transport vesicles. (B–D) Prevalent tip growth defects induced by expression of GFP-Nt-PRK. (B) Balloon tipped and growth arrested. (C) Bifurcated tip; the vacuole-occupied branch (lower, DIC image) was either already growth arrested or likely to cease growth shortly after the image was acquired. (D) A bifurcated GFP-Nt-GFP-expressing pollen tube where growth at both tips had been sustained for some time. Balloon-tipped but not bifurcated tubes were observed previously in LePRK2-transformed pollen tubes (Zhang et al. 2008).

Fig. 3

FER-family RLKs regulating pollen and pistil functions. (A) Single pollen tube entrance in wild-type (left) and supernumerary pollen tube entrance and overgrowth (arrows) in fer ovules (right). (B) As reported in Miyazaki et al. (2009) and Boisson-Dernier et al. (2009), pollen from double anx1 anx2 mutant rupture (arrows, middle panel) immediately or shortly after tube emergence (arrows, lower panel), while wild-type pollen tubes (top panel) elongate efficiently under similar culture conditions.

Fig. 4

A model for FER-mediated RAC/ROP-signalled NADPH oxidase-dependent ROS-regulated polarized cell growth (modified from Duan et al. 2010).