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Genes Nov 2021Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have...
Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-S-RNase and help pollen tubes defend against self-S-RNase. In particular, the contents of putrescine, spermidine, and spermine in the pollen tube treated with self-S-RNase were substantially lower than those treated with non-self-S-RNase. Further analysis of gene expression of key enzymes in the synthesis and degradation pathways of polyamines found that the expression of () as well as several polyamine oxidases such as (), (), and () were significantly up-regulated under self-S-RNase treatment, resulting in the reduction of polyamines. Silencing in pollen tubes alleviates the inhibitory effect of self-S-RNase on pollen tube growth. In addition, exogenous polyamines also enhance pollen tube resistance to self-S-RNase. Transcriptome sequencing data found that polyamines may communicate with S-RNase through the calcium signal pathway, thereby regulating the growth of the pollen tubes. To summarize, our results suggested that polyamines responded to the self-incompatibility reaction and could enhance pollen tube tolerance to S-RNase, thus providing a potential way to break self-incompatibility in apple.
Topics: Malus; Oxidoreductases Acting on CH-NH Group Donors; Plant Proteins; Pollen; Polyamines; Self-Incompatibility in Flowering Plants; Polyamine Oxidase
PubMed: 34828403
DOI: 10.3390/genes12111797 -
Journal of Experimental Botany Apr 2020Pollen tubes rapidly elongate, penetrate, and navigate through multiple female tissues to reach ovules for sperm delivery by utilizing a specialized form of polar growth... (Review)
Review
Pollen tubes rapidly elongate, penetrate, and navigate through multiple female tissues to reach ovules for sperm delivery by utilizing a specialized form of polar growth known as tip growth. This process requires a battery of cellular activities differentially occurring at the apical growing region of the plasma membrane (PM), such as the differential cellular signaling involving calcium (Ca2+), phospholipids, and ROP-type Rho GTPases, fluctuation of ions and pH, exocytosis and endocytosis, and cell wall construction and remodeling. There is an emerging understanding of how at least some of these activities are coordinated and/or interconnected. The apical active ROP modulates exocytosis to the cell apex for PM and cell wall expansion differentially occurring at the tip. The differentiation of the cell wall involves at least the preferential distribution of deformable pectin polymers to the apex and non-deformable pectin polymers to the shank of pollen tubes, facilitating the apical cell expansion driven by high internal turgor pressure. Recent studies have generated inroads into how the ROP GTPase-based intracellular signaling is coordinated spatiotemporally with the external wall mechanics to maintain the tubular cell shape and how the apical cell wall mechanics are regulated to allow rapid tip growth while maintaining the cell wall integrity under the turgor pressure. Evidence suggests that exocytosis and endocytosis play crucial but distinct roles in this spatiotemporal coordination. In this review, we summarize recent advances in the regulation and coordination of the differential pectin distribution and the apical domain of active ROP by exocytosis and endocytosis in pollen tubes.
Topics: Endocytosis; Exocytosis; Pectins; Plants; Pollen Tube; Signal Transduction; rho GTP-Binding Proteins
PubMed: 32173729
DOI: 10.1093/jxb/eraa134 -
The New Phytologist Apr 2019Contents Summary 687 I. Introduction 687 II. Pollen tube membrane-localized receptors coordinate cell integrity and sperm release 689 III. RALF peptides mediate... (Review)
Review
Contents Summary 687 I. Introduction 687 II. Pollen tube membrane-localized receptors coordinate cell integrity and sperm release 689 III. RALF peptides mediate autocrine and paracrine signaling 689 IV. ROS and ion channel signaling mediate intracellular response 690 V. Involvements from pollen tube cell wall components 690 VI. Concluding remarks 691 Acknowledgements 692 Author contributions 692 References 692 SUMMARY: Unlike in animals, sperm in flowering plants are immotile and they are embraced as passive cargoes by a pollen tube which embarks on a long journey in the pistil to deliver them to the female gametophyte for fertilization. How the pollen tube switches from a rapid polarized growth towards its target to an abrupt disintegration for sperm cell release inside the female gametophyte is puzzling. Recent studies have shown that members of the Catharanthus roseus RLK1-like (CrRLK1L) receptor kinase family and their ligands, 5-kDa cysteine-rich peptide rapid alkalinization factors (RALFs), engage in an intricate balancing act involving autocrine and paracrine signaling to maintain pollen tube growth and induce timely tube rupture at the spatially confined pollen tube-female gametophyte interface. Here, we review recent progress related to pollen tube integrity control, mainly focusing on the molecular understanding of signaling as well as intracellular signaling nodes in Arabidopsis. Some missing links and future perspectives are also discussed.
Topics: Magnoliopsida; Peptides; Pollen Tube; Reactive Oxygen Species; Receptors, Cell Surface; Signal Transduction
PubMed: 30556141
DOI: 10.1111/nph.15645 -
Nature Communications May 2020Pollen tubes are highly polarized tip-growing cells that depend on cytosolic pH gradients for signaling and growth. Autoinhibited plasma membrane proton (H) ATPases...
Pollen tubes are highly polarized tip-growing cells that depend on cytosolic pH gradients for signaling and growth. Autoinhibited plasma membrane proton (H) ATPases (AHAs) have been proposed to energize pollen tube growth and underlie cell polarity, however, mechanistic evidence for this is lacking. Here we report that the combined loss of AHA6, AHA8, and AHA9 in Arabidopsis thaliana delays pollen germination and causes pollen tube growth defects, leading to drastically reduced fertility. Pollen tubes of aha mutants had reduced extracellular proton (H) and anion fluxes, reduced cytosolic pH, reduced tip-to-shank proton gradients, and defects in actin organization. Furthermore, mutant pollen tubes had less negative membrane potentials, substantiating a mechanistic role for AHAs in pollen tube growth through plasma membrane hyperpolarization. Our findings define AHAs as energy transducers that sustain the ionic circuit defining the spatial and temporal profiles of cytosolic pH, thereby controlling downstream pH-dependent mechanisms essential for pollen tube elongation, and thus plant fertility.
Topics: Arabidopsis; Arabidopsis Proteins; Cell Membrane; Cell Polarity; Cytosol; Gene Knockdown Techniques; Germination; Hydrogen-Ion Concentration; Membrane Potentials; Mutation; Plants, Genetically Modified; Pollen Tube; Pollination; Protein Isoforms; Proton-Translocating ATPases; Spatio-Temporal Analysis
PubMed: 32409656
DOI: 10.1038/s41467-020-16253-1 -
International Journal of Molecular... Jan 2019Self-incompatibility (SI) is a complex process, one out of several mechanisms that prevent plants from self-fertilizing to maintain and increase the genetic variability.... (Review)
Review
Self-incompatibility (SI) is a complex process, one out of several mechanisms that prevent plants from self-fertilizing to maintain and increase the genetic variability. This process leads to the rejection of the male gametophyte and requires the co-participation of numerous molecules. Plants have evolved two distinct SI systems, the sporophytic (SSI) and the gametophytic (GSI) systems. The two SI systems are markedly characterized by different genes and proteins and each single system can also be divided into distinct subgroups; whatever the mechanism, the purpose is the same, i.e., to prevent self-fertilization. In Malinae, a subtribe in the Rosaceae family, i.e., and , the GSI requires the production of female determinants, known as S-RNases, which penetrate the pollen tube to interact with the male determinants. Beyond this, the penetration of S-RNase into the pollen tube triggers a series of responses involving membrane proteins, such as phospholipases, intracellular variations of cytoplasmic Ca, production of reactive oxygen species (ROS) and altered enzymatic activities, such as that of transglutaminase (TGase). TGases are widespread enzymes that catalyze the post-translational conjugation of polyamines (PAs) to different protein targets and/or the cross-linking of substrate proteins leading to the formation of cross-linked products with high molecular mass. When actin and tubulin are the substrates, this destabilizes the cytoskeleton and inhibits the pollen-tube's growth process. In this review, we will summarize the current knowledge of the relationship between S-RNase penetration, TGase activity and cytoskeleton function during GSI in the Malinae.
Topics: Cytoskeleton; Germ Cells, Plant; Pollen Tube; Rosaceae; Self-Incompatibility in Flowering Plants; Transglutaminases
PubMed: 30626063
DOI: 10.3390/ijms20010209 -
Cytoskeleton (Hoboken, N.J.) Jan 2022The pollen tube is fundamental in the reproduction of seed plants. Particularly in angiosperms, we now have much information about how it grows, how it senses... (Review)
Review
The pollen tube is fundamental in the reproduction of seed plants. Particularly in angiosperms, we now have much information about how it grows, how it senses extracellular signals, and how it converts them into a directional growth mechanism. The expansion of the pollen tube is also related to dynamic cytoplasmic processes based on the cytoskeleton (such as polymerization/depolymerization of microtubules and actin filaments) or motor activity along with the two cytoskeletal systems and is dependent on motor proteins. While a considerable amount of information is available for the actomyosin system in the pollen tube, the role of microtubules in the transport of organelles or macromolecular structures is still quite uncertain despite that 30 years ago the first work on the presence of kinesins in the pollen tube was published. Since then, progress has been made in elucidating the role of kinesins in plant cells. However, their role within the pollen tube is still enigmatic. In this review, I will postulate some roles of kinesins in the pollen tube 30 years after their initial discovery based on information obtained in other plant cells in the meantime. The most concrete hypotheses predict that kinesins in the pollen tube enable the short movement of specific organelles or contribute to generative cell or sperm cell transport, as well as mediate specific steps in the process of endocytosis.
Topics: Actomyosin; Kinesins; Microtubules; Pollen Tube; Seeds
PubMed: 35766009
DOI: 10.1002/cm.21713 -
Nature Communications Jan 2023Pollen tube guidance within female tissues of flowering plants can be divided into preovular guidance, ovular guidance and a connecting stage called pollen tube...
Pollen tube guidance within female tissues of flowering plants can be divided into preovular guidance, ovular guidance and a connecting stage called pollen tube emergence. As yet, no female factor has been identified to positively regulate this transition process. In this study, we show that an ovary-expressed bHLH transcription factor Cucumis sativus ALCATRAZ (CsALC) functions in pollen tube emergence in cucumber. CsALC knockout mutants showed diminished pollen tube emergence, extremely reduced entry into ovules, and a 95% reduction in female fertility. Further examination showed two rapid alkalinization factors CsRALF4 and CsRALF19 were less expressed in Csalc ovaries compared to WT. Besides the loss of male fertility derived from precocious pollen tube rupture as in Arabidopsis, Csralf4 Csralf19 double mutants exhibited a 60% decrease in female fertility due to reduced pollen tube distribution and decreased ovule targeting efficiency. In brief, CsALC regulates female fertility and promotes CsRALF4/19 expression in the ovary during pollen tube guidance in cucumber.
Topics: Cucumis sativus; Ovary; Pollen Tube; Arabidopsis; Arabidopsis Proteins; Ovule
PubMed: 36650145
DOI: 10.1038/s41467-023-35936-z -
Frontiers in Plant Science 2020The male-female interactions in pollination mediate pollen hydration and germination, pollen tube growth and fertilization. Reactive oxygen species (ROS) derived from... (Review)
Review
The male-female interactions in pollination mediate pollen hydration and germination, pollen tube growth and fertilization. Reactive oxygen species (ROS) derived from both male and female tissues play regulatory roles for the communication between the pollen/pollen tube and female tissues at various stages, such as pollen hydration and germination on the stigma, pollen tube growth in the pistil and pollen tube reception in the female gametophyte. In this minireview, we primarily summarize the recent progress on the roles of ROS signaling in male-female interactions during pollination and discuss several ROS-regulated downstream signaling pathways for these interactions. Furthermore, several ROS-involved downstream pathways are outlined, such as Ca signaling, cell wall cytomechanics, the redox modification of CRP, and cell PCD. At the end, we address the roles of ROS in pollen tube guidance and fertilization as future questions that merit study.
PubMed: 32180782
DOI: 10.3389/fpls.2020.00177 -
Frontiers in Plant Science 2016Plants, unlike animals, alternate multicellular diploid, and haploid generations in their life cycle. While this is widespread all along the plant kingdom, the size and... (Review)
Review
Plants, unlike animals, alternate multicellular diploid, and haploid generations in their life cycle. While this is widespread all along the plant kingdom, the size and autonomy of the diploid sporophyte and the haploid gametophyte generations vary along evolution. Vascular plants show an evolutionary trend toward a reduction of the gametophyte, reflected both in size and lifespan, together with an increasing dependence from the sporophyte. This has resulted in an overlooking of the importance of the gametophytic phase in the evolution of higher plants. This reliance on the sporophyte is most notorious along the pollen tube journey, where the male gametophytes have to travel a long way inside the sporophyte to reach the female gametophyte. Along evolution, there is a change in the scenery of the pollen tube pathway that favors pollen competition and selection. This trend, toward apparently making complicated what could be simple, appears to be related to an increasing control of the sporophyte over the gametophyte with implications for understanding plant evolution.
PubMed: 26904071
DOI: 10.3389/fpls.2016.00107 -
Plant Physiology Jul 2016Root hair cells and pollen tubes, like fungal hyphae, possess a typical tip or polar cell expansion with growth limited to the apical dome. Cell expansion needs to be... (Review)
Review
Root hair cells and pollen tubes, like fungal hyphae, possess a typical tip or polar cell expansion with growth limited to the apical dome. Cell expansion needs to be carefully regulated to produce a correct shape and size. Polar cell growth is sustained by oscillatory feedback loops comprising three main components that together play an important role regulating this process. One of the main components are reactive oxygen species (ROS) that, together with calcium ions (Ca(2+)) and pH, sustain polar growth over time. Apoplastic ROS homeostasis controlled by NADPH oxidases as well as by secreted type III peroxidases has a great impact on cell wall properties during cell expansion. Polar growth needs to balance a focused secretion of new materials in an extending but still rigid cell wall in order to contain turgor pressure. In this review, we discuss the gaps in our understanding of how ROS impact on the oscillatory Ca(2+) and pH signatures that, coordinately, allow root hair cells and pollen tubes to expand in a controlled manner to several hundred times their original size toward specific signals.
Topics: Calcium; Cell Membrane; Cell Polarity; Cytoplasm; Homeostasis; Hydrogen-Ion Concentration; Peroxidases; Plant Cells; Plant Proteins; Plant Roots; Pollen Tube; Reactive Oxygen Species
PubMed: 27208283
DOI: 10.1104/pp.16.00191