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Cell Aug 2023Animal 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...
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.
Topics: Animals; Arabidopsis; Arabidopsis Proteins; Fertilization; Pollen Tube; Seeds; Germ Cells, Plant
PubMed: 37516107
DOI: 10.1016/j.cell.2023.06.024 -
International Journal of Molecular... Feb 2023The aim of this Special Issue is to highlight the molecular dialogue between the pollen tube and the pistil [...].
The aim of this Special Issue is to highlight the molecular dialogue between the pollen tube and the pistil [...].
Topics: Pollen Tube; Cell Communication; Pollination; Flowers
PubMed: 36835118
DOI: 10.3390/ijms24043707 -
Cell Oct 2023Pollen-pistil interactions establish interspecific/intergeneric pre-zygotic hybridization barriers in plants. The rejection of undesired pollen at the stigma is crucial...
Pollen-pistil interactions establish interspecific/intergeneric pre-zygotic hybridization barriers in plants. The rejection of undesired pollen at the stigma is crucial to avoid outcrossing but can be overcome with the support of mentor pollen. The mechanisms underlying this hybridization barrier are largely unknown. Here, in Arabidopsis, we demonstrate that receptor-like kinases FERONIA/CURVY1/ANJEA/HERCULES RECEPTOR KINASE 1 and cell wall proteins LRX3/4/5 interact on papilla cell surfaces with autocrine stigmatic RALF1/22/23/33 peptide ligands (sRALFs) to establish a lock that blocks the penetration of undesired pollen tubes. Compatible pollen-derived RALF10/11/12/13/25/26/30 peptides (pRALFs) act as a key, outcompeting sRALFs and enabling pollen tube penetration. By treating Arabidopsis stigmas with synthetic pRALFs, we unlock the barrier, facilitating pollen tube penetration from distantly related Brassicaceae species and resulting in interspecific/intergeneric hybrid embryo formation. Therefore, we uncover a "lock-and-key" system governing the hybridization breadth of interspecific/intergeneric crosses in Brassicaceae. Manipulating this system holds promise for facilitating broad hybridization in crops.
Topics: Arabidopsis; Arabidopsis Proteins; Brassicaceae; Peptide Hormones; Peptides; Pollen; Pollen Tube; Reproductive Isolation
PubMed: 37806310
DOI: 10.1016/j.cell.2023.09.003 -
Science (New York, N.Y.) Jan 2022Fertilization of an egg by multiple sperm (polyspermy) leads to lethal genome imbalance and chromosome segregation defects. In , the block to polyspermy is facilitated...
Fertilization of an egg by multiple sperm (polyspermy) leads to lethal genome imbalance and chromosome segregation defects. In , the block to polyspermy is facilitated by a mechanism that prevents polytubey (the arrival of multiple pollen tubes to one ovule). We show here that FERONIA, ANJEA, and HERCULES RECEPTOR KINASE 1 receptor-like kinases located at the septum interact with pollen tube-specific RALF6, 7, 16, 36, and 37 peptide ligands to establish this polytubey block. The same combination of RALF (rapid alkalinization factor) peptides and receptor complexes controls pollen tube reception and rupture inside the targeted ovule. Pollen tube rupture releases the polytubey block at the septum, which allows the emergence of secondary pollen tubes upon fertilization failure. Thus, orchestrated steps in the fertilization process in are coordinated by the same signaling components to guarantee and optimize reproductive success.
Topics: Arabidopsis; Arabidopsis Proteins; Fertilization; Ligands; Ovule; Peptides; Phosphotransferases; Pollen; Pollen Tube; Pollination; Protein Kinases; Signal Transduction
PubMed: 35050671
DOI: 10.1126/science.abl4683 -
Science (New York, N.Y.) Nov 2023Assembly of cell wall polysaccharides into specific patterns is required for plant growth. A complex of RAPID ALKALINIZATION FACTOR 4 (RALF4) and its cell wall-anchored...
Assembly of cell wall polysaccharides into specific patterns is required for plant growth. A complex of RAPID ALKALINIZATION FACTOR 4 (RALF4) and its cell wall-anchored LEUCINE-RICH REPEAT EXTENSIN 8 (LRX8)-interacting protein is crucial for cell wall integrity during pollen tube growth, but its molecular connection with the cell wall is unknown. Here, we show that LRX8-RALF4 complexes adopt a heterotetrametric configuration in vivo, displaying a dendritic distribution. The LRX8-RALF4 complex specifically interacts with demethylesterified pectins in a charge-dependent manner through RALF4's polycationic surface. The LRX8-RALF4-pectin interaction exerts a condensing effect, patterning the cell wall's polymers into a reticulated network essential for wall integrity and expansion. Our work uncovers a dual structural and signaling role for RALF4 in pollen tube growth and in the assembly of complex extracellular polymers.
Topics: Arabidopsis; Cell Wall; Pectins; Peptides; Pollen Tube; Arabidopsis Proteins
PubMed: 37943924
DOI: 10.1126/science.adi4720 -
International Journal of Molecular... Nov 2021Angiosperm mature pollen represents a quiescent stage with a desiccated cytoplasm surrounded by a tough cell wall, which is resistant to the suboptimal environmental... (Review)
Review
Angiosperm mature pollen represents a quiescent stage with a desiccated cytoplasm surrounded by a tough cell wall, which is resistant to the suboptimal environmental conditions and carries the genetic information in an intact stage to the female gametophyte. Post pollination, pollen grains are rehydrated, activated, and a rapid pollen tube growth starts, which is accompanied by a notable metabolic activity, synthesis of novel proteins, and a mutual communication with female reproductive tissues. Several angiosperm species (, tobacco, maize, and kiwifruit) were subjected to phosphoproteomic studies of their male gametophyte developmental stages, mostly mature pollen grains. The aim of this review is to compare the available phosphoproteomic studies and to highlight the common phosphoproteins and regulatory trends in the studied species. Moreover, the pollen phosphoproteome was compared with root hair phosphoproteome to pinpoint the common proteins taking part in their tip growth, which share the same cellular mechanisms.
Topics: Phosphoproteins; Plant Proteins; Pollen Tube; Pollination; Proteome; Proteomics
PubMed: 34830092
DOI: 10.3390/ijms222212212 -
Frontiers in Plant Science 2022Double fertilization is a unique and particularly complicated process for the generation alternation of angiosperms. Sperm cells of angiosperms lose the motility... (Review)
Review
Double fertilization is a unique and particularly complicated process for the generation alternation of angiosperms. Sperm cells of angiosperms lose the motility compared with that of gymnosperms. The sperm cells are passively carried and transported by the pollen tube for a long journey before targeting the ovule. Two sperm cells are released at the cleft between the egg and the central cell and fused with two female gametes to produce a zygote and endosperm, respectively, to accomplish the so-called double fertilization process. In this process, extensive communication and interaction occur between the male (pollen or pollen tube) and the female (ovule). It is suggested that small peptides and receptor kinases play critical roles in orchestrating this cell-cell communication. Here, we illuminate the understanding of phases in the process, such as pollen-stigma recognition, the hydration and germination of pollen grains, the growth, guidance, and rupture of tubes, the release of sperm cells, and the fusion of gametes, by reviewing increasing data recently. The roles of peptides and receptor kinases in signaling mechanisms underlying cell-cell communication were focused on, and directions of future studies were perspected in this review.
PubMed: 36589119
DOI: 10.3389/fpls.2022.1090836 -
Trends in Plant Science Aug 2021Plant signaling peptides are involved in cell-cell communication networks and coordinate a wide range of plant growth and developmental processes. Signaling peptides... (Review)
Review
Plant signaling peptides are involved in cell-cell communication networks and coordinate a wide range of plant growth and developmental processes. Signaling peptides generally bind to receptor-like kinases, inducing their dimerization with co-receptors for signaling activation to trigger cellular signaling and biological responses. Fertilization is an important life event in flowering plants, involving precise control of cell-cell communications between male and female tissues. Peptide-receptor-like kinase-mediated signaling plays an important role in male-female interactions for successful fertilization in flowering plants. Here, we describe the recent findings on the functions and signaling pathways of peptides and receptors involved in plant reproduction processes including pollen germination, pollen tube growth, pollen tube guidance to the embryo sac, and sperm cell reception in female tissues.
Topics: Genes, Plant; Peptides; Pollen Tube; Pollination; Reproduction; Signal Transduction
PubMed: 33715959
DOI: 10.1016/j.tplants.2021.02.008 -
Annual Review of Plant Biology Apr 2020Fertilization of flowering plants requires the organization of complex tasks, many of which become integrated by the female gametophyte (FG). The FG is a few-celled... (Review)
Review
Fertilization of flowering plants requires the organization of complex tasks, many of which become integrated by the female gametophyte (FG). The FG is a few-celled haploid structure that orchestrates division of labor to coordinate successful interaction with the sperm cells and their transport vehicle, the pollen tube. As reproductive outcome is directly coupled to evolutionary success, the underlying mechanisms are under robust molecular control, including integrity check and repair mechanisms. Here, we review progress on understanding the development and function of the FG, starting with the functional megaspore, which represents the haploid founder cell of the FG. We highlight recent achievements that have greatly advanced our understanding of pollen tube attraction strategies and the mechanisms that regulate plant hybridization and gamete fusion. In addition, we discuss novel insights into plant polyploidization strategies that expand current concepts on the evolution of flowering plants.
Topics: Fertilization; Magnoliopsida; Ovule; Pollen Tube
PubMed: 32442389
DOI: 10.1146/annurev-arplant-081519-035943 -
Plants (Basel, Switzerland) Jun 2021Pollen germination and pollen tube growth are common to all seed plants, but these processes first developed in gymnosperms and still serve for their successful sexual... (Review)
Review
Pollen germination and pollen tube growth are common to all seed plants, but these processes first developed in gymnosperms and still serve for their successful sexual reproduction. The main body of data on the reproductive physiology, however, was obtained on flowering plants, and one should be careful to extrapolate the discovered patterns to gymnosperms. In recent years, physiological studies of coniferous pollen have been increasing, and both the features of this group and the similarities with flowering plants have already been identified. The main part of the review is devoted to physiological studies carried out on conifer pollen. The main properties and diversity of pollen grains and pollination strategies in gymnosperms are described.
PubMed: 34206892
DOI: 10.3390/plants10071301