Central-cell-produced attractants control fertilization recovery.

Animal fertilization relies on hundreds of sperm racing toward the egg, whereas, in angiosperms, only two sperm cells are delivered by a pollen tube to the female gametes (egg cell and central cell) for double fertilization. However, unsuccessful fertilization under this one-pollen-tube design can be detrimental to seed production and plant survival. To mitigate this risk, unfertilized-gamete-controlled extra pollen tube entry has been evolved to bring more sperm cells and salvage fertilization. Despite its importance, the underlying molecular mechanism of this phenomenon remains unclear. In this study, we report that, in Arabidopsis, the central cell secretes peptides SALVAGER1 and SALVAGER2 in a directional manner to attract pollen tubes when the synergid-dependent attraction fails or is terminated by pollen tubes carrying infertile sperm cells. Moreover, loss of SALs impairs the fertilization recovery capacity of the ovules. Therefore, this research uncovers a female gamete-attraction system that salvages seed production for reproductive assurance.

POD1-SUN-CRT3 chaperone complex guards the ER sorting of LRR receptor kinases in Arabidopsis.

Protein sorting in the secretory pathway is essential for cellular compartmentalization and homeostasis in eukaryotic cells. The endoplasmic reticulum (ER) is the biosynthetic and folding factory of secretory cargo proteins. The cargo transport from the ER to the Golgi is highly selective, but the molecular mechanism for the sorting specificity is unclear. Here, we report that three ER membrane localized proteins, SUN3, SUN4 and SUN5, regulate ER sorting of leucine-rich repeat receptor kinases (LRR-RKs) to the plasma membrane. The triple mutant sun3/4/5 displays mis-sorting of these cargo proteins to acidic compartments and therefore impairs the growth of pollen tubes and the whole plant. Furthermore, the extracellular LRR domain of LRR-RKs is responsible for the correct sorting. Together, this study reports a mechanism that is important for the sorting of cell surface receptors.

Integration of ovular signals and exocytosis of a Ca2+ channel by MLOs in pollen tube guidance.

The spatiotemporal regulation of Ca2+ channels at the plasma membrane in response to extracellular signals is critical for development, stress response and reproduction, but is poorly understood. During flowering-plant reproduction, pollen tubes grow directionally to the ovule, which is guided by ovule-derived signals and dependent on Ca2+ dynamics. However, it is unknown how ovular signals are integrated with cytosolic Ca2+ dynamics in the pollen tube. Here, we show that MILDEW RESISTANCE LOCUS O 5 (MLO5), MLO9 and MLO15 are required for pollen tube responses to ovular signals in Arabidopsis thaliana. Phenotypically distinct from the ovule-bypass phenotype of previously identified mutants, mlo5 mlo9 double-mutant and mlo5 mlo9 mlo15 triple-mutant pollen tubes twist and pile up after sensing the ovular cues. Molecular studies reveal that MLO5 and MLO9 selectively recruit Ca2+ channel CNGC18-containing vesicles to the plasma membrane through the R-SNARE proteins VAMP721 and VAMP722 in trans mode. This study identifies members of the conserved seven transmembrane MLO family (expressed in the pollen tube) as tethering factors for Ca2+ channels, reveals a novel mechanism of molecular integration of extracellular ovular cues and selective exocytosis, and sheds light on the general regulation of MLO proteins in cell responses to environmental stimuli.

TICKET attracts pollen tubes and mediates reproductive isolation between relative species in Brassicaceae.

In flowering plants, pollen tubes are attracted to the ovule by secreted peptides to release the sperm cells for double fertilization. This process is species-specific and acts as an important stage of reproductive isolation between species. Here we identified a cysteine-rich peptide TICKET2 in Arabidopsis thaliana and its orthologs in Arabidopsis lyrata and Capsella rebella that can attract the conspecific pollen tubes, but not the pollen tubes of relative species in Brassicaceae. Genetic knockout of the AtTICKET subclade compromised the pollen tube attraction efficiency. This study identified a new pollen tube attracting signal and shed light on the molecular basis of reproductive isolation.

Multilayered signaling pathways for pollen tube growth and guidance.

Sexual reproductive success is essential for the survival of all higher organisms. As the most prosperous and diverse group of land plants on earth, flowering plants evolved highly sophisticated fertilization mechanisms. To adapt to the terrestrial environment, a tubular structure pollen tube has been evolved to deliver the immobile sperm cells to the egg and central cell enclosed within the ovule. The pollen tube is generated from the vegetative cell of the pollen (male gametophyte), where two sperm cells are hosted. Pollen tube elongation in the maternal tissue and navigation to the ovule require intimate cell-cell interactions between the tube and female tissues. Questions on how the single-celled pollen tube accomplishes such task and how the female tissues accommodate the tube have attracted many plant biologists. Here, we review recent progresses and concepts in understanding the molecular mechanisms governing pollen tube growth and its interactions with the female tissues. We will also discuss the future perspective in this field.