Abstract
The regulation of pollen development and pollen tube growth is a complicated biological process that is crucial for sexual reproduction in flowering plants. Annexins are widely distributed from protists to higher eukaryotes and play multiple roles in numerous cellular events by acting as a putative “linker” between Ca2+ signaling, the actin cytoskeleton and the membrane, which are required for pollen development and pollen tube growth. Our recent report suggested that downregulation of the function of Arabidopsis annexin 5 (Ann5) in transgenic Ann5-RNAi lines caused severely sterile pollen grains. However, little is known about the underlying mechanisms of the function of Ann5 in pollen. This study demonstrated that Ann5 associates with phospholipid membrane and this association is stimulated by Ca2+ in vitro. Brefeldin A (BFA) interferes with endomembrane trafficking and inhibits pollen germination and pollen tube growth. Both pollen germination and pollen tube growth of Ann5-overexpressing plants showed increased resistance to BFA treatment, and this effect was regulated by calcium. Overexpression of Ann5 promoted Ca2+-dependent cytoplasmic streaming in pollen tubes in vivo in response to BFA. Lactrunculin (LatB) significantly prohibited pollen germination and tube growth by binding with high affinity to monomeric actin and preferentially targeting dynamic actin filament arrays and preventing actin polymerization. Overexpression of Ann5 did not affect pollen germination or pollen tube growth in response to LatB compared with wild-type, although Ann5 interacts with actin filaments in a manner similar to some animal annexins. In addition, the sterile pollen phenotype could be only partially rescued by Ann5 mutants at Ca2+-binding sites when compared to the complete recovery by wild-type Ann5. These data demonstrated that Ann5 is involved in pollen development, germination and pollen tube growth through the promotion of endomembrane trafficking modulated by calcium. Our results provide reliable molecular mechanisms that underlie the function of Ann5 in pollen.
Highlights
Pollen germination and pollen tube growth are key steps in the double fertilization sexual reproduction process of flowering plants [1]
Calcium ions bind to the convex side of the core and face the membrane when annexin 5 (Ann5) binds to phospholipids
A similar tendency was found for the pollen tube growth of the Ann5-overexpressing lines in response to Brefeldin A (BFA) treatment (Table 1). These results demonstrated that pollen germination and pollen tube growth of Ann5-overexpressing plants significantly increased the resistance to BFA treatment compared with the wild-type, which implied that Ann5 was involved in endomembrane trafficking and most likely promoted processes in response to BFA stimulation via binding to negatively charged phospholipids
Summary
Pollen germination and pollen tube growth are key steps in the double fertilization sexual reproduction process of flowering plants [1]. Many signaling molecules and cellular events, including Ca2+, pH, phosphatidyl inositol, endocytosis, exocytosis, vesicle trafficking, plasma membrane fusion and actin filament reorganization, have been shown to be separately or synergistically involved in regulating the accurate polarized growth of the pollen tube [2]. Some recent studies have shown that the actin cytoskeleton in the pollen tube functions as a track for vesicle trafficking and directs the distribution of vesicles [6]. If this actin cytoskeleton was destroyed, vesicles would not be accurately transported to the specific locus of the membrane at the apex, causing the pollen tubes to stop growing [14]. Little is known about the underlying mechanisms that regulate pollen development and pollen tube growth via the coordinated regulation of the membrane, actin cytoskeleton and Ca2+ because the functional ‘‘linkers‘‘ between these factors remain unknown
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