-
Journal of Integrative Plant Biology Jul 2023Pollen tube polar growth is a key physiological activity for angiosperms to complete double fertilization, which is highly dependent on the transport of polar substances...
Pollen tube polar growth is a key physiological activity for angiosperms to complete double fertilization, which is highly dependent on the transport of polar substances mediated by secretory vesicles. The exocyst and Sec1/Munc18 (SM) proteins are involved in the regulation of the tethering and fusion of vesicles and plasma membranes, but the molecular mechanism by which they regulate pollen tube polar growth is still unclear. In this study, we found that loss of function of SEC1A, a member of the SM protein family in Arabidopsis thaliana, resulted in reducing pollen tube growth and a significant increase in pollen tube width. SEC1A was diffusely distributed in the pollen tube cytoplasm, and was more concentrated at the tip of the pollen tube. Through co-immunoprecipitation-mass spectrometry screening, protein interaction analysis and in vivo microscopy, we found that SEC1A interacted with the exocyst subunit SEC6, and they mutually affected the distribution and secretion rate at the tip of the pollen tube. Meanwhile, the functional loss of SEC1A and SEC6 significantly affected the distribution of the SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) complex member SYP125 at the tip of the pollen tube, and led to the disorder of pollen tube cell wall components. Genetic analysis revealed that the pollen tube-related phenotype of the sec1a sec6 double mutant was significantly enhanced compared with their respective single mutants. Therefore, we speculated that SEC1A and SEC6 cooperatively regulate the fusion of secretory vesicles and plasma membranes in pollen tubes, thereby affecting the length and the width of pollen tubes.
Topics: Arabidopsis; Arabidopsis Proteins; Cell Cycle; Cell Membrane; Pollen Tube
PubMed: 36951316
DOI: 10.1111/jipb.13486 -
International Journal of Molecular... Nov 2021In angiosperms, double fertilization requires pollen tubes to transport non-motile sperm to distant egg cells housed in a specialized female structure known as the... (Review)
Review
In angiosperms, double fertilization requires pollen tubes to transport non-motile sperm to distant egg cells housed in a specialized female structure known as the pistil, mediating the ultimate fusion between male and female gametes. During this journey, the pollen tube encounters numerous physical barriers that must be mechanically circumvented, including the penetration of the stigmatic papillae, style, transmitting tract, and synergid cells as well as the ultimate fusion of sperm cells to the egg or central cell. Additionally, the pollen tube must maintain structural integrity in these compact environments, while responding to positional guidance cues that lead the pollen tube to its destination. Here, we discuss the nature of these physical barriers as well as efforts to genetically and cellularly identify the factors that allow pollen tubes to successfully, specifically, and quickly circumnavigate them.
Topics: Cell Communication; Flowers; Pollen Tube; Pollination
PubMed: 34830110
DOI: 10.3390/ijms222212230 -
Journal of Integrative Plant Biology Sep 2023Pollen tube growth is essential for successful double fertilization, which is critical for grain yield in crop plants. Rapid alkalinization factors (RALFs) function as...
Pollen tube growth is essential for successful double fertilization, which is critical for grain yield in crop plants. Rapid alkalinization factors (RALFs) function as ligands for signal transduction during fertilization. However, functional studies on RALF in monocot plants are lacking. Herein, we functionally characterized two pollen-specific RALFs in rice (Oryza sativa) using multiple clustered regularly interspaced palindromic repeats (CRISPR)/CRISPR-associated protein 9-induced loss-of-function mutants, peptide treatment, expression analyses, and tag reporter lines. Among the 41 RALF members in rice, OsRALF17 was specifically expressed at the highest level in pollen and pollen tubes. Exogenously applied OsRALF17 or OsRALF19 peptide inhibited pollen tube germination and elongation at high concentrations but enhanced tube elongation at low concentrations, indicating growth regulation. Double mutants of OsRALF17 and OsRALF19 (ralf17/19) exhibited almost full male sterility with defects in pollen hydration, germination, and tube elongation, which was partially recovered by exogenous treatment with OsRALF17 peptide. This study revealed that two partially functionally redundant OsRALF17 and OsRALF19 bind to Oryza sativa male-gene transfer defective 2 (OsMTD2) and transmit reactive oxygen species signals for pollen tube germination and integrity maintenance in rice. Transcriptomic analysis confirmed their common downstream genes, in osmtd2 and ralf17/19. This study provides new insights into the role of RALF, expanding our knowledge of the biological role of RALF in regulating rice fertilization.
Topics: Pollen Tube; Oryza; Pollen; Signal Transduction; Peptides
PubMed: 37195059
DOI: 10.1111/jipb.13508 -
Annual Review of Plant Biology Jun 2021Pollen-pistil interactions serve as important prezygotic reproductive barriers that play a critical role in mate selection in plants. Here, we highlight recent progress...
Pollen-pistil interactions serve as important prezygotic reproductive barriers that play a critical role in mate selection in plants. Here, we highlight recent progress toward understanding the molecular basis of pollen-pistil interactions as reproductive isolating barriers. These barriers can be active systems of pollen rejection, or they can result from a mismatch of required male and female factors. In some cases, the barriers are mechanistically linked to self-incompatibility systems, while others represent completely independent processes. Pollen-pistil reproductive barriers can act as soon as pollen is deposited on a stigma, where penetration of heterospecific pollen tubes is blocked by the stigma papillae. As pollen tubes extend, the female transmitting tissue can selectively limit growth by producing cell wall-modifying enzymes and cytotoxins that interact with the growing pollen tube. At ovules, differential pollen tube attraction and inhibition of sperm cell release can act as barriers to heterospecific pollen tubes.
Topics: Flowers; Pollen; Pollen Tube; Pollination; Reproduction
PubMed: 34143652
DOI: 10.1146/annurev-arplant-080620-102159 -
The Plant Cell Sep 2022Pollen tube guidance regulates the growth direction and ovule targeting of pollen tubes in pistils, which is crucial for the completion of sexual reproduction in...
Pollen tube guidance regulates the growth direction and ovule targeting of pollen tubes in pistils, which is crucial for the completion of sexual reproduction in flowering plants. The Arabidopsis (Arabidopsis thaliana) pollen-specific receptor kinase (PRK) family members PRK3 and PRK6 are specifically tip-localized and essential for pollen tube growth and guidance. However, the mechanisms controlling the polar localization of PRKs at the pollen tube tip are unclear. The Arabidopsis P4-ATPase ALA3 helps establish the polar localization of apical phosphatidylserine (PS) in pollen tubes. Here, we discovered that loss of ALA3 function caused pollen tube defects in growth and ovule targeting and significantly affected the polar localization pattern of PRK3 and PRK6. Both PRK3 and PRK6 contain two polybasic clusters in the intracellular juxtamembrane domain, and they bound to PS in vitro. PRK3 and PRK6 with polybasic cluster mutations showed reduced or abolished binding to PS and altered polar localization patterns, and they failed to effectively complement the pollen tube-related phenotypes of prk mutants. These results suggest that ALA3 influences the precise localization of PRK3, PRK6, and other PRKs by regulating the distribution of PS, which plays a key role in regulating pollen tube growth and guidance.
Topics: Adenosine Triphosphatases; Arabidopsis; Arabidopsis Proteins; Phosphatidylserines; Phospholipids; Pollen Tube; Protein Serine-Threonine Kinases
PubMed: 35861414
DOI: 10.1093/plcell/koac208 -
Plant Communications Nov 2023Heat waves induced by climate warming have become common in food-producing regions worldwide, frequently coinciding with high temperature (HT)-sensitive stages of many... (Review)
Review
Heat waves induced by climate warming have become common in food-producing regions worldwide, frequently coinciding with high temperature (HT)-sensitive stages of many crops and thus threatening global food security. Understanding the HT sensitivity of reproductive organs is currently of great interest for increasing seed set. The responses of seed set to HT involve multiple processes in both male and female reproductive organs, but we currently lack an integrated and systematic summary of these responses for the world's three leading food crops (rice, wheat, and maize). In the present work, we define the critical high temperature thresholds for seed set in rice (37.2°C ± 0.2°C), wheat (27.3°C ± 0.5°C), and maize (37.9°C ± 0.4°C) during flowering. We assess the HT sensitivity of these three cereals from the microspore stage to the lag period, including effects of HT on flowering dynamics, floret growth and development, pollination, and fertilization. Our review synthesizes existing knowledge about the effects of HT stress on spikelet opening, anther dehiscence, pollen shedding number, pollen viability, pistil and stigma function, pollen germination on the stigma, and pollen tube elongation. HT-induced spikelet closure and arrest of pollen tube elongation have a catastrophic effect on pollination and fertilization in maize. Rice benefits from pollination under HT stress owing to bottom anther dehiscence and cleistogamy. Cleistogamy and secondary spikelet opening increase the probability of pollination success in wheat under HT stress. However, cereal crops themselves also have protective measures under HT stress. Lower canopy/tissue temperatures compared with air temperatures indicate that cereal crops, especially rice, can partly protect themselves from heat damage. In maize, husk leaves reduce inner ear temperature by about 5°C compared with outer ear temperature, thereby protecting the later phases of pollen tube growth and fertilization processes. These findings have important implications for accurate modeling, optimized crop management, and breeding of new varieties to cope with HT stress in the most important staple crops.
Topics: Temperature; Edible Grain; Pollination; Hot Temperature; Seeds; Crops, Agricultural
PubMed: 37226443
DOI: 10.1016/j.xplc.2023.100629 -
Trends in Plant Science Dec 2019Understanding the molecular basis of pollen germination in cereals holds great potential to improve yield. Pollen, a highly specialized haploid male gametophyte,... (Review)
Review
Understanding the molecular basis of pollen germination in cereals holds great potential to improve yield. Pollen, a highly specialized haploid male gametophyte, transports sperm cells through a pollen tube to the female ovule for fertilization, directly determining grain yield in cereal crops. Although insights into the regulation of pollen germination and gamete interaction have advanced rapidly in the model Arabidopsis thaliana (arabidopsis), the molecular mechanisms in monocot cereals remain largely unknown. Recently, pollen-specific genome-wide and mutant analyses in rice and maize have extended our understanding of monocot regulatory components. We highlight conserved and diverse mechanisms underlying pollen hydration, germination, and tube growth in cereals that provide ideas for translating this research from arabidopsis. Recent developments in gene-editing systems may facilitate further functional genetic research.
Topics: Arabidopsis; Arabidopsis Proteins; Edible Grain; Germination; Pollen; Pollen Tube
PubMed: 31610991
DOI: 10.1016/j.tplants.2019.08.005 -
Planta Jan 2021In flowering plants, pollen germination on the stigma and pollen tube growth in pistil tissues are critical for sexual plant reproduction, which are involved in the... (Review)
Review
In flowering plants, pollen germination on the stigma and pollen tube growth in pistil tissues are critical for sexual plant reproduction, which are involved in the interactions between pollen/pollen tube and pistil tissues. GPI-anchored proteins (GPI-APs) are located on the external surface of the plasma membrane and function in various processes of sexual plant reproduction. The evidences suggest that GPI-APs participate in endosome machinery, Ca oscillations, the development of the transmitting tract, the maintenance of the integrity of pollen tube, the enhancement of interactions of the receptor-like kinase (RLK) and ligand, and guidance of the growth of pollen tube, and so on. In this review, we will summarize the recent progress on the roles of GPI-APs in the interactions between pollen/pollen tube and pistil tissues during pollination, such as pollen germination on the stigma, pollen tube growth in the transmitting tract, pollen tube guidance to the ovule, and pollen tube reception in the embryo sac. We will also discuss the future outlook of GPI-APs in the interactions between pollen/pollen tube and pistil tissues.
Topics: Flowers; GPI-Linked Proteins; Ovule; Plant Proteins; Pollen Tube; Pollination; Research
PubMed: 33394122
DOI: 10.1007/s00425-020-03526-8 -
Frontiers in Plant Science 2021
PubMed: 33719326
DOI: 10.3389/fpls.2021.658902 -
Frontiers in Plant Science 2020Pollen tube (PT) serves as a vehicle that delivers male gametes (sperm cells) to a female gametophyte during double fertilization, which eventually leads to the seed... (Review)
Review
Pollen tube (PT) serves as a vehicle that delivers male gametes (sperm cells) to a female gametophyte during double fertilization, which eventually leads to the seed formation. It is one of the fastest elongating structures in plants. Normally, PTs traverse through the extracellular matrix at the transmitting tract after penetrating the stigma. While the endeavor may appear simple, the molecular processes and mechanics of the PT elongation is yet to be fully resolved. Although it is the most studied "tip-growing" structure in plants, several features of the structure (e.g., Membrane dynamics, growth behavior, mechanosensing etc.) are only partially understood. In many aspects, PTs are still considered as a tissue rather than a "unique cell." In this review, we have attempted to discuss mainly on the mechanics behind PT-elongation and briefly on the molecular players involved in the process. Four aspects of PTs are particularly discussed: the PT as a cell, its membrane dynamics, mechanics of its elongation, and the potential mechanosensors involved in its elongation based on relevant findings in both plant and non-plant models.
PubMed: 33193543
DOI: 10.3389/fpls.2020.589712