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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 -
Plant Communications Apr 2024In angiosperms, the pollen tube enters the receptive synergid cell, where it ruptures to release its cytoplasm along with two sperm cells. This interaction is complex,...
In angiosperms, the pollen tube enters the receptive synergid cell, where it ruptures to release its cytoplasm along with two sperm cells. This interaction is complex, and the exact signal transducers that trigger the bursting of pollen tubes are not well understood. In this study, we identify three homologous receptor-like cytoplasmic kinases (RLCKs) expressed in pollen tubes of Arabidopsis, Delayed Burst 1/2/3 (DEB1/2/3), which play a crucial role in this process. These genes produce proteins localized on the plasma membrane, and their knockout causes delayed pollen tube burst and entrance of additional pollen tubes into the embryo sac due to fertilization recovery. We show that DEBs interact with the Ca pump ACA9, influencing the dynamics of cytoplasmic Ca in pollen tubes through phosphorylation. These results highlight the importance of DEBs as key signal transducers and the critical function of the DEB-ACA9 axis in timely pollen tube burst in synergids.
PubMed: 38689493
DOI: 10.1016/j.xplc.2024.100934 -
Plants (Basel, Switzerland) Aug 2023Embryo rescue (ER) techniques are among the oldest and most successful in vitro tissue culture protocols used with plant species. ER refers to a series of methods that... (Review)
Review
Embryo rescue (ER) techniques are among the oldest and most successful in vitro tissue culture protocols used with plant species. ER refers to a series of methods that promote the development of an immature or lethal embryo into a viable plant. Intraspecific, interspecific, or intergeneric crosses allow the introgression of important alleles of agricultural interest from wild species, such as resistance or tolerance to abiotic and biotic stresses or morphological traits in crops. However, pre-zygotic and post-zygotic reproductive barriers often present challenges in achieving successful hybridization. Pre-zygotic barriers manifest as incompatibility reactions that hinder pollen germination, pollen tube growth, or penetration into the ovule occurring in various tissues, such as the stigma, style, or ovary. To overcome these barriers, several strategies are employed, including cut-style or graft-on-style techniques, the utilization of mixed pollen from distinct species, placenta pollination, and in vitro ovule pollination. On the other hand, post-zygotic barriers act at different tissues and stages ranging from early embryo development to the subsequent growth and reproduction of the offspring. Many crosses among different genera result in embryo abortion due to the failure of endosperm development. In such cases, ER techniques are needed to rescue these hybrids. ER holds great promise for not only facilitating successful crosses but also for obtaining haploids, doubled haploids, and manipulating the ploidy levels for chromosome engineering by monosomic and disomic addition as well substitution lines. Furthermore, ER can be used to shorten the reproductive cycle and for the propagation of rare plants. Additionally, it has been repeatedly used to study the stages of embryonic development, especially in embryo-lethal mutants. The most widely used ER procedure is the culture of immature embryos taken and placed directly on culture media. In certain cases, the in vitro culture of ovule, ovaries or placentas enables the successful development of young embryos from the zygote stage to maturity.
PubMed: 37687352
DOI: 10.3390/plants12173106 -
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 -
Frontiers in Plant Science 2023
PubMed: 37496862
DOI: 10.3389/fpls.2023.1242416 -
Biochemical Society Transactions Dec 2023Plant organelles predominantly rely on the actin cytoskeleton and the myosin motors for long-distance trafficking, while using microtubules and the kinesin motors mostly...
Plant organelles predominantly rely on the actin cytoskeleton and the myosin motors for long-distance trafficking, while using microtubules and the kinesin motors mostly for short-range movement. The distribution and motility of organelles in the plant cell are fundamentally important to robust plant growth and defense. Chloroplasts, mitochondria, and peroxisomes are essential organelles in plants that function independently and coordinately during energy metabolism and other key metabolic processes. In response to developmental and environmental stimuli, these energy organelles modulate their metabolism, morphology, abundance, distribution and motility in the cell to meet the need of the plant. Consistent with their metabolic links in processes like photorespiration and fatty acid mobilization is the frequently observed inter-organellar physical interaction, sometimes through organelle membranous protrusions. The development of various organelle-specific fluorescent protein tags has allowed the simultaneous visualization of organelle movement in living plant cells by confocal microscopy. These energy organelles display an array of morphology and movement patterns and redistribute within the cell in response to changes such as varying light conditions, temperature fluctuations, ROS-inducible treatments, and during pollen tube development and immune response, independently or in association with one another. Although there are more reports on the mechanism of chloroplast movement than that of peroxisomes and mitochondria, our knowledge of how and why these three energy organelles move and distribute in the plant cell is still scarce at the functional and mechanistic level. It is critical to identify factors that control organelle motility coupled with plant growth, development, and stress response.
Topics: Organelles; Actin Cytoskeleton; Peroxisomes; Chloroplasts; Mitochondria; Microtubules
PubMed: 37975429
DOI: 10.1042/BST20221093 -
Trends in Plant Science Mar 2024Plant reproduction is a complex, highly-coordinated process in which a single, male germ cell grows through the maternal reproductive tissues to reach and fertilise the... (Review)
Review
Plant reproduction is a complex, highly-coordinated process in which a single, male germ cell grows through the maternal reproductive tissues to reach and fertilise the egg cell. Focussing on Arabidopsis thaliana, we review signalling between male and female partners which is important throughout the pollen tube journey, especially during pollen tube reception at the ovule. Numerous receptor kinases and their coreceptors are implicated in signal perception in both the pollen tube and synergid cells at the ovule entrance, and several specific peptide and carbohydrate ligands for these receptors have recently been identified. Clarifying the interplay between these signals and the downstream responses they instigate presents a challenge for future research and may help to illuminate broader principles of plant cell-cell communication.
Topics: Pollen Tube; Signal Transduction; Arabidopsis; Arabidopsis Proteins; Fertilization
PubMed: 37640641
DOI: 10.1016/j.tplants.2023.07.011 -
EMBO Reports Jun 2024In the pistil of flowering plants, each ovule usually associates with a single pollen tube for fertilization. This one-to-one pollen tube guidance, which contributes to...
In the pistil of flowering plants, each ovule usually associates with a single pollen tube for fertilization. This one-to-one pollen tube guidance, which contributes to polyspermy blocking and efficient seed production, is largely different from animal chemotaxis of many sperms to one egg. However, the functional mechanisms underlying the directional cues and polytubey blocks in the depths of the pistil remain unknown. Here, we develop a two-photon live imaging method to directly observe pollen tube guidance in the pistil of Arabidopsis thaliana, clarifying signaling and cellular behaviors in the one-to-one guidance. Ovules are suggested to emit multiple signals for pollen tubes, including an integument-dependent directional signal that reaches the inner surface of the septum and adhesion signals for emerged pollen tubes on the septum. Not only FERONIA in the septum but ovular gametophytic FERONIA and LORELEI, as well as FERONIA- and LORELEI-independent repulsion signal, are involved in polytubey blocks on the ovular funiculus. However, these funicular blocks are not strictly maintained in the first 45 min, explaining previous reports of polyspermy in flowering plants.
Topics: Pollen Tube; Arabidopsis; Signal Transduction; Ovule; Arabidopsis Proteins; Fertilization
PubMed: 38773320
DOI: 10.1038/s44319-024-00151-4 -
Plants (Basel, Switzerland) Jul 2023Intergeneric and interspecific hybridization has been employed for the breeding of to transfer desirable traits between species, producing novel phenotypes with...
Intergeneric and interspecific hybridization has been employed for the breeding of to transfer desirable traits between species, producing novel phenotypes with improved size, color, form, and flower-bearing ability. These characteristics are often enhanced; however, many of these hybrids are triploids and have reduced or complete sterility, for example, Queen Beer 'Mantefon', an important novelty-type cultivar in Asia, particularly in China, Japan, and Republic of Korea. Despite the increasing demand for the crop for ornamental purposes, little is known about its cytogenetics, which is essential for breeding and, consequently, crop improvement. In this study, karyotyping using fluorescence in situ hybridization, meiotic chromosome behavior analysis, pollen staining, and in vitro viability germination tests were performed to understand the cause of hybrid sterility and pollen abnormality in Queen Beer 'Mantefon' from a cytogenetic perspective. Viability tests revealed pollen infertility at all flower developmental stages, confirmed by the absence of pollen tube growth. Aberrant chromosomal behavior was observed in pollen mother cells (PMCs), frequently forming univalents, chromosomal bridges, and laggards during the entire meiotic process. PMCs were also divided irregularly into sporads with varying numbers of micronuclei, which may be responsible for pollen sterility in this cultivar. Altogether, the cytogenetic analyses provided insights into the pollen development of Queen Beer 'Mantefon' and the conceivable causes of its infertility.
PubMed: 37570982
DOI: 10.3390/plants12152828 -
Plants (Basel, Switzerland) Mar 2024Alfalfa ( L.) is an important forage crop worldwide, but molecular genetics and breeding research in this species are hindered by its self-incompatibility (SI). Although...
Alfalfa ( L.) is an important forage crop worldwide, but molecular genetics and breeding research in this species are hindered by its self-incompatibility (SI). Although the mechanisms underlying SI have been extensively studied in other plant families, SI in legumes, including alfalfa, remains poorly understood. Here, we determined that self-pollinated pollen tubes could germinate on the stigma of alfalfa, grow through the style, and reach the ovarian cavity, but the ovules collapsed ~48 h after self-pollination. A transcriptomic analysis of dissected pistils 24 h after self-pollination identified 941 differently expressed genes (DEGs), including 784 upregulated and 157 downregulated genes. A gene ontology (GO) analysis showed that the DEGs were highly enriched in functions associated with the regulation of pollen tube growth and pollen germination. A Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis indicated that pentose and glucuronate interconversion, plant hormone signal transduction, the spliceosome, and ribosomes might play important roles in SI. Our co-expression analysis showed that F-box proteins, serine/threonine protein kinases, calcium-dependent protein kinases (CDPKs), bHLHs, bZIPs, and MYB-related family proteins were likely involved in the SI response. Our study provides a catalog of candidate genes for further study to understand SI in alfalfa and related legumes.
PubMed: 38592914
DOI: 10.3390/plants13060875