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Plant Signaling & Behavior Aug 2021Following pollen deposition on the receptive surface of the stigma, pollen germinates a tube that carries male gametes toward the ovule where fertilization occurs. As...
Following pollen deposition on the receptive surface of the stigma, pollen germinates a tube that carries male gametes toward the ovule where fertilization occurs. As soon as it emerges from the pollen grain, the pollen tube has to be properly guided through the pistil tissues so as to reach the ovule and ensure double fertilization. Chemical attractants, nutrients as well as receptor kinase-dependent signaling pathways have been implicated in this guidance. Recently, we showed in Arabidopsis that the microtubule severing enzyme KATANIN, by acting both on cortical microtubule (CMT) dynamics and cellulose microfibril (CMF) deposition, conferred particular mechanical properties to the papilla cell wall that act as active guidance factors. Here we confirm the importance of KATANIN and CMT orientation in pollen tube directionality by examining another mutant.
Topics: Arabidopsis; Arabidopsis Proteins; Cell Wall; Cellulose; Fertilization; Flowers; Katanin; Microtubules; Ovule; Pollen; Pollen Tube; Pollination
PubMed: 33960266
DOI: 10.1080/15592324.2021.1921992 -
Plant Physiology Apr 2021Recent insights into the mechanism of pollen tube growth and guidance point to the importance of H dynamics, which are regulated by the plasma membrane H-ATPase. (Review)
Review
Recent insights into the mechanism of pollen tube growth and guidance point to the importance of H dynamics, which are regulated by the plasma membrane H-ATPase.
Topics: Cell Differentiation; Cell Membrane; Cell Proliferation; Plant Physiological Phenomena; Pollen Tube; Proton-Translocating ATPases
PubMed: 33793904
DOI: 10.1093/plphys/kiaa092 -
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 -
Plant Biotechnology Journal Sep 2023In angiosperms, the timely delivery of sperm cell nuclei by pollen tube (PT) to the ovule is vital for double fertilization. Penetration of PT into maternal stigma...
In angiosperms, the timely delivery of sperm cell nuclei by pollen tube (PT) to the ovule is vital for double fertilization. Penetration of PT into maternal stigma tissue is a critical step for sperm cell nuclei delivery, yet little is known about the process. Here, a male-specific and sporophytic mutant xt6, where PTs are able to germinate but unable to penetrate the stigma tissue, is reported in Oryza sativa. Through genetic study, the causative gene was identified as Chalcone synthase (OsCHS1), encoding the first enzyme in flavonoid biosynthesis. Indeed, flavonols were undetected in mutant pollen grains and PTs, indicating that the mutation abolished flavonoid biosynthesis. Nevertheless, the phenotype cannot be rescued by exogenous application of quercetin and kaempferol as reported in maize and petunia, suggesting a different mechanism exists in rice. Further analysis showed that loss of OsCHS1 function disrupted the homeostasis of flavonoid and triterpenoid metabolism and led to the accumulation of triterpenoid, which inhibits significantly α-amylase activity, amyloplast hydrolysis and monosaccharide content in xt6, these ultimately impaired tricarboxylic acid (TCA) cycle, reduced ATP content and lowered the turgor pressure as well. Our findings reveal a new mechanism that OsCHS1 modulates starch hydrolysis and glycometabolism through modulating the metabolic homeostasis of flavonoids and triterpenoids which affects α-amylase activity to maintain PT penetration in rice, which contributes to a better understanding of the function of CHS1 in crop fertility and breeding.
Topics: Pollen Tube; Flavonoids; Oryza; Plant Breeding; Seeds; Homeostasis; Starch; alpha-Amylases
PubMed: 37221659
DOI: 10.1111/pbi.14073 -
Plant Signaling & Behavior 2015Experimental evidences support that the circadian rhythm regulates the transcription levels of genes encoding the enzymes involved in plant metabolism. However, there is... (Review)
Review
Experimental evidences support that the circadian rhythm regulates the transcription levels of genes encoding the enzymes involved in plant metabolism. However, there is no paper to refer the correlation of the circadian rhythms and the metabolic processes for facilitating pollen tube growth. In this study, we found that many central components of the circadian clock were highly enriched and specifically present in the in vivo grown Arabidopsis pollen tubes. Our analysis also identified the significant differentially expressed genes encoding co-expressed enzymes in the consecutive steps of fatty acid β-oxidation II, pentose phosphate pathway (oxidative branch) and phosphatidic acid biosynthesis pathway in the in vivo grown Arabidopsis pollen tubes during pollination. Thus, it is implicated that the circadian rhythms of pollen tube may be adjusted and have a greater probability of the direct or indirect functional relationship with enhanced intracellular Ca(2+) dynamics and ATP production for facilitating pollen tube growth in vivo.
Topics: Adenosine Triphosphate; Arabidopsis; Calcium; Circadian Rhythm; Pollen Tube
PubMed: 26039479
DOI: 10.1080/15592324.2015.1017699 -
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 -
The Plant Journal : For Cell and... Apr 2021Non-specific phospholipase Cs (NPCs) are responsible for membrane lipid remodeling that involves hydrolysis of the polar head group of membrane phospholipids....
Non-specific phospholipase Cs (NPCs) are responsible for membrane lipid remodeling that involves hydrolysis of the polar head group of membrane phospholipids. Arabidopsis NPC2 and NPC6 are essential in gametogenesis, but their underlying role in the lipid remodeling remains elusive. Here, we show that these NPCs are required for triacylglycerol (TAG) production in pollen tube growth. NPC2 and NPC6 are highly expressed in developing pollen tubes and are localized at the endoplasmic reticulum. Mutants of NPC2 and NPC6 showed reduced rate of pollen germination, length of pollen tube and amount of lipid droplets (LDs). Overexpression of NPC2 or NPC6 induced LD accumulation, which suggests that these NPCs are involved in LD production. Furthermore, mutants defective in the biosynthesis of TAG, a major component of LDs, showed defective pollen tube growth. These results suggest that NPC2 and NPC6 are essential in gametogenesis for a role in hydrolyzing phospholipids and producing TAG required for pollen tube growth. Thus, lipid remodeling from phospholipids to TAG during pollen tube growth represents an emerging role for the NPC family in plant developmental control.
Topics: Arabidopsis; Arabidopsis Proteins; Flowers; Phospholipases; Pollen Tube; Triglycerides; Type C Phospholipases
PubMed: 33506578
DOI: 10.1111/tpj.15172 -
Annals of Botany Sep 2011In contrast to animals and lower plants such as mosses and ferns, sperm cells of flowering plants (angiosperms) are immobile and require transportation to the female... (Review)
Review
BACKGROUND
In contrast to animals and lower plants such as mosses and ferns, sperm cells of flowering plants (angiosperms) are immobile and require transportation to the female gametes via the vegetative pollen tube cell to achieve double fertilization. The path of the pollen tube towards the female gametophyte (embryo sac) has been intensively studied in many intra- and interspecific crossing experiments with the aim of increasing the gene pool of crop plants for greater yield, improved biotic and abiotic stress resistance, and for introducing new agronomic traits. Many attempts to hybridize different species or genotypes failed due to the difficulty for the pollen tubes in reaching the female gametophyte. Detailed studies showed that these processes are controlled by various self-incompatible (intraspecific) and cross-incompatible (interspecific) hybridization mechanisms.
SCOPE
Understanding the molecular mechanisms of crossing barriers is therefore of great interest in plant reproduction, evolution and breeding research. In particular, pre-zygotic hybridization barriers related to pollen tube germination, growth, guidance and sperm delivery, which are considered the major hybridization controls in nature and thus also contribute to species isolation and speciation, have been intensively investigated. Despite this general interest, surprisingly little is known about these processes in the most important agronomic plant family, the Gramineae, Poaceae or grasses. Small polymorphic proteins and their receptors, degradation of sterility locus proteins and general compounds such as calcium, γ-aminobutyric acid or nitric oxide have been shown to be involved in progamic pollen germination, adhesion, tube growth and guidance, as well as sperm release. Most advances have been made in the Brassicaceae, Papaveraceae, Linderniaceae and Solanaceae families including their well-understood self-incompatibility (SI) systems. Grass species evolved similar mechanisms to control the penetration and growth of self-pollen to promote intraspecific outcrossing and to prevent fertilization by alien sperm cells. However, in the Poaceae, the underlying molecular mechanisms are still largely unknown.
CONCLUSIONS
We propose to develop maize (Zea mays) as a model to investigate the above-described processes to understand the associated intra- and interspecific crossing barriers in grasses. Many genetic, cellular and biotechnological tools including the completion of a reference genome (inbred line B73) have been established in the last decade and many more maize inbred genomes are expected to be available soon. Moreover, a cellular marker line database as well as large transposon insertion collections and improved Agrobacterium transformation protocols are now available. Additionally, the processes described above are well studied at the morphological level and a number of mutants have been described already, awaiting disclosure of the relevant genes. The identification of the first key players in pollen tube growth, guidance and burst show maize to be an excellent grass model to investigate these processes in more detail. Here we provide an overview of our current understanding of these processes in Poaceae with a focus on maize, and also include relevant discoveries in eudicot model species.
Topics: Amino Acid Sequence; Germination; Models, Biological; Molecular Sequence Data; Plant Proteins; Pollen Tube; Self-Incompatibility in Flowering Plants; Zea mays
PubMed: 21345919
DOI: 10.1093/aob/mcr017 -
EMBO Reports Feb 2020Communication between the gametophytes is vital for angiosperm fertilisation. Multiple CrRLK1L-type receptor kinases prevent premature pollen tube burst, while another...
Communication between the gametophytes is vital for angiosperm fertilisation. Multiple CrRLK1L-type receptor kinases prevent premature pollen tube burst, while another CrRLK1L protein, FERONIA (FER), is required for pollen tube reception in the female gametophyte. We report here the identification of two additional CrRLK1L homologues, HERCULES RECEPTOR KINASE 1 (HERK1) and ANJEA (ANJ), which act redundantly to promote pollen tube growth arrest at the synergid cells. HERK1 and ANJ localise to the filiform apparatus of the synergid cells in unfertilised ovules, and in herk1 anj mutants, a majority of ovules remain unfertilised due to pollen tube overgrowth, together indicating that HERK1 and ANJ act as female determinants for fertilisation. As in fer mutants, the synergid cell-specific, endomembrane protein NORTIA (NTA) is not relocalised after pollen tube reception; however, unlike fer mutants, reactive oxygen species levels are unaffected in herk1 anj double mutants. Both ANJ and HERK1 associate with FER and its proposed co-receptor LORELEI (LRE) in planta. Together, our data indicate that HERK1 and ANJ act with FER to mediate female-male gametophyte interactions during plant fertilisation.
Topics: Arabidopsis; Arabidopsis Proteins; Phosphotransferases; Pollen Tube; Protein Kinases; Signal Transduction
PubMed: 31867824
DOI: 10.15252/embr.201948466